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Adaptive radiation: the interaction of ecological opportunity, adaptation, and speciation

January 2010

January 2010

Authors:

Jonathan B Losos

Washington University in St. Louis

D. Luke Mahler

University of Toronto

Adaptive radiation of island Birds (A) Hawaiian honeycreepers exhibit stunning morphological disparity in bill traits which corresponds to diversity in resource use. (B) The disparity of honeycreepers surpasses that of their mainland relatives, the cardueline finches and rivals that of all passerine birds. Another island radiation, Darwin's finches, also exhibits substantial disparity. In both island radiations, species occupy a diverse range of ecological niches utilized by species in many different families on the mainland. (A, reproduced with permission from Pratt 2005; B, adapted from Lovette et al. 2002 and Losos and Ricklefs 2009.)

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The relationship between divergent Adaptation and reproductive isolation The more dissimilar two species are in habitat use, the greater the degree of reproductive isolation that has evolved between them. Each point represents the degree of difference between two closely related species or populations. (Adapted from Funk et al. 2006.)

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Peak Shifts along an Adaptive ridge (A) The ancestral species occurs on the lower adaptive peak on Island A. Because an adaptive valley lies between the two peaks, natural selection cannot drive the population to the second peak. (B) However, on Island B, an adaptive ridge connects the ancestral position to a higher peak, and when individuals immigrate to Island B from Island A, the new population on Island B evolves a new morphology. Subsequently, the population on Island B evolves reproductive isolation. When individuals from Island B then recolonize Island A, they may evolve to the second peak on that island, leading to the coexistence of two species-one on each adaptive peak. (Adapted from Schluter 2000.)

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Selection for Background Matching in the Walking Stick, Timema cristinae Experimental studies of selection reveal that in the presence of avian predators, dull stripes, and bright bodies ("brightness contrast" is body brightness minus stripe brightness) are favored in the Ceanothus ecotype (A) and bright stripes and dull bodies in the Adenostoma ecotype (B). In the absence of predators, selection does not differ between insects on the two bushes (C and D). (Adapted from Nosil and Crespi 2006.)

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Chapter 15

Adaptive Radiation: The Interaction of

Ecological Opportunity, Adaptation,

and Speciation

Jonathan B. Losos and D. Luke Mahler

Darwin may have been the first to describe adaptive radiation when, con-

templating the variety of finches that now bear his name, he remarked:

“Seeing this gradation and diversity of structure in one small, intimately

related group of birds, one might really fancy that from an original paucity

of birds in this archipelago, one species has been taken and modified for

different ends” (Darwin 1845: 380). Since Darwin’s time, naturalists and

evolutionary biologists have been fascinated by the extraordinary diversity

of ecology, morphology, behavior, and species richness of some clades, but

interest in adaptive radiation has surged in recent years, largely as a result

of three developments.

First, evolutionary ecologists have focused on the mechanisms that pro-

duce adaptive radiation. Careful study of ecological divergence within and

among populations has yielded a wealth of information about how natu-

ral selection leads to evolutionary diversification (Schluter 2003; Nosil and

Crespi 2006; Grant and Grant 2008a) ( Figure 15.1). Schluter’s (2000) seminal

work, The Ecology of Adaptive Radiation was a watershed in the field, build-

ing upon and extending in important ways Simpson’s (1953) The Major

Features of Evolution published a half-century earlier.

Second, the explosion of molecular phylogenetics in the last two decades

(see Hillis, Chapter 16) has revealed the diversification histories of count-

less clades and has provided the raw material for a renaissance of adaptive

radiation studies. Molecular research has offered surprising discoveries

about the history and magnitude of many adaptive radiations, such as the

vangids of Madagascar (Yamagishi et al. 2001) (Figure 15.2), the corvoids

of Australia (Sibley and Ahlquist 1990; Barker et al. 2004), the cichlids of

Lake Victoria (Meyer et al. 1990; Seehausen 2006), the lobeliads of Hawaii

(Givnish et al. 2009) and a plethora of others. In each of these cases, the great

ecological and morphological diversity of a group had been thought to be

the result of independent colonization events from multiple, differently

adapted ancestral lineages. Instead, new molecular phylogenies revealed

382 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 383

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that the great diversity in these groups is the result of in situ evolution, that

is, adaptive radiation (see references previously cited).

Not only have many previously unknown adaptive radiations been dis-

covered with molecular data, but also time-calibrated phylogenetic trees

of extant taxa allow classic hypotheses of adaptive radiation to be tested in

new ways (Glor 2010). Previously, the primary way to estimate the tempo

of macroevolution was to measure it directly using high-quality paleon-

tological data (see Wagner, Chapter 17), which are available for relatively

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Figure 15.01 Date 04-19-10

75 9 11 13 15 17

(B)

Growth rate in open water (mg/d)

Growth rate in littoral zone (mg/d)

Benthic

Hybrid

Limnetic

–1.5 –1.0 –0.5 0.0 0.5 1.0 1.5

3.8

3.9

4.0

3.7

(C)

Morphological index

Logarithm of growth rate (mm per 90 days)

(A)

Figure 15.1 Natural Selection and Adaptation in British Columbian

Threespine Sticklebacks (Gasterosteus aculeatus) (A) A number of lakes in

British Columbia contain two species of sticklebacks, one that is slender-bodied,

with a small mouth, eats zooplankton, and occupies open water (limnetic,

above); the other is larger, deeper-bodied, has a large mouth, and eats inverte-

brates near the lake bottom (benthic, below). (B) Each species has higher growth

rates in its own habitat, and hybrids are inferior in both habitats. (C) Natural

selection (using growth rate as a proxy) on a highly variable hybrid population

favors more benthic-like individuals in the presence of the limnetic species (red

dots and solid line), but not in their absence (green dots and dashed line). Such

studies have shed light on the role of ecology and natural selection in driving

divergence during adaptive radiation. (A, from Rundle and Schluter 2004, photos

Figure 15.2 Malagasy Vangids Molecular phylogenetic study indicates that the

vangids represent a monophyletic group, rather than being members of several dif-

ferent families with closest relatives elsewhere. (From Yamagishi et al. 2001.)

384 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 385

in any form without express written permission from the publisher.

few lineages. However, nucleotide sequence data now provide an alter-

native means of reconstructing phylogenetic relationships and the timing

of lineage divergence events. With time-calibrated phylogenies, one may

ask questions such as whether the occurrence of adaptive radiation is cor-

related with historical events (e.g., mass extinctions, changes in climate)

or whether the pace of diversification decreases through time, as often is

expected of an adaptive radiation (Box 15.1).

Third, experimental studies of microbial evolution have added a new

dimension to the study of adaptive radiation (see Dykhuizen, Commentary

2). Such studies bring the benefits of experimental control, large sample

sizes and replication, and the ability to not only track lineages through the

diversification process, but also to freeze ancestral taxa and subsequently

resurrect them to interact with their descendants (Lenski and Travisano

1994). Although thus far primarily based on studies of short-lived asexually

reproducing organisms diversifying under simplified ecological conditions

(a situation that is changing), microbial evolution studies have permitted

experimental tests of many of the basic hypotheses of adaptive radiation,

allowing microevolutionary processes to be directly and experimentally

connected to macroevolutionary outcomes and often confirming predic-

tions of the adaptive radiation model (Kassen 2009) (Figure 15.3).

With time-calibrated phylogenies, researchers

can investigate whether lineage diversiﬁcation

patterns match patterns expected from the

ecological process of adaptive radiation. These

approaches focus on how the pace of lineage

or phenotypic diversiﬁcation alters over time or

with changing ecological conditions, such as eco-

logical opportunity. The most common approach

to testing for the signature of adaptive radiation

is to construct models in which parameters de-

scribe changes in the tempo of diversiﬁcation as

a result of ecological conditions. Alternative eco-

logical models may be compared to each other,

to non-ecological models, or to a null model in

which diversiﬁcation proceeds at a constant rate.

Tests for the signature of adaptive radiation

have a rich pedigree in quantitative paleontol-

ogy, in which numerous studies have tracked the

rise and fall of diversity and disparity in relation

to mass extinction events, the evolution of key

innovations, and colonization of new regions

(Simpson 1953; Sepkoski 1978; Foote 1997,

1999; reviewed in Erwin 2007; see Foote, Chap-

ter 18) (Figure 1A,B).

Box 15.1

TESTING FOR CHARACTERISTIC PATTERNS OF ADAPTIVE RADIATION

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Figure 15.03 Date 04-19-10

It is very difficult to

see what is happening

in the tubes.

(A) Heterogeneous environment

(B) Homogeneous environment

Figure 15.3 Experiments on the

Evolutionary Diversification of the Bacterium

Pseudomonas fluorescens Resources were

distributed either heterogeneously (solu-

tion with red and green strata in A) or

homogeneously (uniform green solution in

B) distributed. After several days, bacteria

in the heterogeneous environments repeat-

edly diverged into the same three morpho-

types, which interact negatively and differ

in resource use (the yellow shading on the

right depicts typical resource use for each

morphotype; the different forms tend to

thrive as a surface film, in solution, or along

the substrate, respectively). By contrast, only

one morphotype occurred in the homog-

enous treatment. (Adapted from Rainey and

Travisano 1998.)

Figure 1 The “Early Burst” Pattern of Adap-

tive Radiation In the fossil record, an early

burst may be detected by tracking the number

of species and the total disparity of a radiation

over geological time. In trilobites, species rich-

ness (A) and disparity (B) both peaked early in

the history of the clade. Phylogenetic compara-

tive methods may be used to detect an early

burst from data on extant taxa. Greater Antil-

lean Anolis lizards exhibit both a rapid early

accumulation of lineages, depicted as a concave

lineages-through-time plot in (C), as well as an

early burst in phenotypic evolution, evident as

larger independent contrasts early in the radia-

tion (D). (A,B adapted from Foote 1993; C,D

adapted from Mahler et al. 2010.)

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Figure Box 15.01 Date 04-19-10

0 0.000

497560 434 371 308 245

258

515

773

1031

1288

Geologic time (Ma)

Number of species

(A)

497560 434 371 308 245

0.014

0.028

0.043

0.057

0.071

–100 –80 –60 –40 –20 0

Relative time before present

Limb length contrasts

(absolute value)

(D)

Geologic time (Ma)

Disparity

(B)

–100 –80 –60 –40 –20 0

100

Relative time before present

Log (lineages)

(C)

(continued)

386 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 387

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In this chapter, we review what is known about the mechanisms that

drive adaptive radiation and, more importantly, highlight those areas re-

quiring further research. Along the way, we will discuss what constitutes

an adaptive radiation and how one can be identified.

Evolutionary Radiation: What Are the Types, How Are

They Recognized, and Are They Special?

Adaptive radiations draw the attention of scientists and non-scientists alike

because their grandeur seems to imply that something special is respon-

sible: these groups are extraordinary and require explanation, invocation

of some special attribute, either intrinsic or external, that can explain why

these particular clades have diversified to such an extreme extent (Box

15.2). But, adaptive radiation describes only one part of the spectrum of

evolutionary radiations. Although distinguishing among types of evolu-

tionary radiation may involve making arbitrary distinctions (Olson and

Arroyo-Santos 2009), doing so provides a useful framework for further

study of the key features of radiations.

The most commonly used phylogenetic test

evaluates the early burst model, in which early

diversiﬁcation is explosive as lineages rapidly

adapt to new ecological roles but slows as op-

portunities disappear due to ecological satura-

tion (Nee et al. 1992; Rabosky and Lovette 2008;

Phillimore and Price 2009; reviewed in Glor

2010). The majority of tests of the “early burst”

model have investigated patterns of lineage

diversiﬁcation, but similar models have recently

been developed for phenotypic traits as well

(Freckleton and Harvey 2006; Agrawal et al. 2009;

Harmon et al. 2010, in press; Mahler et al. 2010,

in revision) (Figure 1C,D). Support for this model

varies—the common ﬁnding of temporally de-

clining lineage diversiﬁcation has led some to

proclaim a strong role for ecological opportunity

in regulating cladogenesis, although the sample

of clades studied may be biased (McPeek 2008;

Phillimore and Price 2008; Ricklefs 2009). Among

phenotypic studies of the early burst model

(which, to date, are far fewer than studies focus-

ing on species richness), some studies report

declining rates of evolution with diminishing

ecological opportunity (Freckleton and Harvey

2006; Agrawal et al. 2009; Mahler et al. 2010, in

revision), whereas Harmon et al. (2010) ﬁnd only

limited support for the early burst model in a

wide survey of animal radiations.

A key feature of the model-ﬁtting approach is

the ﬂexibility provided by the variety of models

that may be compared when evaluating adap-

tive radiation hypotheses. In addition to the ear-

ly burst model, a diversity of alternative models

are available for ﬁtting data, including radiation

under ﬂexible ecological limits, radiation with

high lineage turnover, and radiation in stages,

among others (Price 1997; Harvey and Rambaut

2000; McPeek 2008; Benton 2009; Gavrilets and

Vose 2009; Rabosky 2009). The ability to identify

patterns of adaptive radiation using phylogenet-

ic methods is likely to improve in coming years

as new and more reﬁned models are developed.

Box 15.1 Continued

We suggest that the term adaptive radiation

should be reserved for those clades exhibiting

exceptional ecological and phenotypic disparity

(see Figure 15.4). The rationale for this argument

is that it is the unusually great degree of dispar-

ity in these clades that requires explanation—by

identifying such clades, researchers can focus on

them to understand what has triggered their ex-

traordinary evolutionary diversiﬁcation. Implicit

in this approach is the need to develop statistical

methods to separate those clades that constitute

adaptive radiations from those that do not.

This approach can be criticized on two

counts. First, it creates an arbitrary dichotomy

in what is most likely a continuous distribution

(Olson and Arroyo-Santos 2009). That is, the de-

gree of adaptive disparity of clades is surely con-

tinuously distributed. How can one draw a line

and say that all clades with a greater amount of

disparity than the threshold constitute adaptive

radiations and that all with even a slightly lesser

amount, are not?

An alternative approach to the threshold-

based approach would be to quantify disparity

for a sample of clades and investigate whether

the degree of disparity is statistically related to

a factor, such as degree of ecological opportu-

nity (presuming it could be quantiﬁed), that has

been hypothesized to drive adaptive radiation.

Increasingly, tools for investigating the relation-

ship between such factors and patterns of eco-

logical diversiﬁcation are being developed and

employed (Olson and Arroyo-Santos 2009; Glor

2010).

The second criticism of this deﬁnition of

adaptive radiation is based on the view that

adaptive radiation is a process as well as an out-

come (just as one might argue that adaptation is

both a process and an end-result). This argument

suggests that the same processes are involved in

adaptive diversiﬁcation whether the result is an

enormous adaptive radiation, such as African Rift

Lake cichlids, or a small clade of species slightly

morphologically diﬀerentiated to adapt to minor

diﬀerences in habitat use. Because both cases

are the result of the same process of cladogen-

esis plus adaptive divergence driven by natural

selection, this view would suggest that all such

clades, no matter how disparate, should be con-

sidered adaptive radiations.

Such a view would render the term adap-

tive radiation meaningless. The vast majority

of clades are composed of species that exhibit

at least a small degree of phenotypic disparity

that has arisen as a result of adaptive divergence

driven by natural selection. Assuming this is true,

almost all clades would be adaptive radiations,

and the term would have little utility in identify-

ing clades of special interest. We feel that this

not only neuters the term “adaptive radiation,”

but also departs from its use throughout the his-

tory of evolutionary biology.

One way out of this problem might be to

restrict the term adaptive radiation to clades in

which adaptive diversity arose in a burst of evo-

lution early in a clade’s history, with subsequent

deceleration in the rate of evolution. Indeed,

many deﬁnitions of adaptive radiation include

the proviso that radiation must occur quickly

(Givnish 1997). This view, however, also has prob-

lems. Either the deﬁnition must include clades

that achieve only modest disparity as long as

they accumulated it early, or it must rely on an

arbitrary disparity threshold.

From our perspective and that of many others

(Givnish 1997), the important aspect of adaptive

radiation is the disparity produced by the clade

(Foote 1997; Erwin 2007), rather than the pace at

which it accumulates. In some models of adap-

tive radiation (Harvey and Rambaut 2000), an

adaptive radiation may unfold at a rather steady

pace; indeed, ecological opportunity may ap-

Box 15.2

ARE ADAPTIVE RADIATIONS EXCEPTIONAL?

(continued)

388 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 389

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Evolutionary radiation results in the production of two components of di-

versity—species richness and phenotypic diversity (often termed “disparity”

to avoid confusion with “species diversity”). Adaptive radiation is a type of

evolutionary radiation, emphasizing the extent of phenotypic differentiation

among members of a clade as species adapt to use different ecological re-

sources; we henceforth refer to this as “adaptive disparity.” Although a wide

variety of definitions of adaptive radiation have been proposed (Givnish

1997), Futuyma’s (1998) definition seems to capture the sense of most of

these: “evolutionary divergence of members of a single phylogenetic lineage

into a variety of different adaptive forms.” More specifically, we propose

that the term adaptive radiation should refer to those clades that exhibit an

exceptional extent of adaptive disparity. Definitional issues and methods for

identifying adaptive radiations are reviewed in Box 15.3.1

Much of the literature on evolutionary radiations equates species rich-

ness with adaptive radiation. Indeed, many of the world’s most remark-

able and celebrated radiations are rich in both species and adaptive form,

including the African Rift Lake cichlids, Hawaiian Drosophila, Caribbean

Anolis lizards and, at a higher level, beetles and angiosperms. Such lineages

undoubtedly represent adaptive radiations and suggest that species prolif-

eration and ecological radiation occur hand in hand. Although often true,

this need not be the case.

Some clades are exceptionally diverse phenotypically and constitute

adaptive radiations, despite having unexceptional species diversity (Fig-

ure 15.4). For example, the lizard clades Pygopodidae and Cordylidae both

contain great ecological and morphological disparity despite being spe-

cies poor (Webb and Shine 1994; Branch 1998). Groups such as these are

commonly neglected in studies of adaptive radiation, but deserve more

1 Integral to the concept of adaptive radiation is the concept of adaptation

itself. Evolutionary divergence can occur for reasons other than adaptive

differentiation. Thus, investigation of the adaptive basis of trait differentiation

is essential in any study of adaptive radiation. Arnold (1994), Larson and

Losos (1996), and McPeek, Commentary 3 (in this volume) provide reviews of

adaptation and how it can be studied. For the purposes of discussion here, we

will assume that phenotypic differences among species are adaptively based.

attention, particularly in studies of the role of speciation in adaptive radia-

tion (see subsequent discussion).

Conversely, other clades contain a great number of species, but little eco-

logical or phenotypic disparity. For example, the eastern North American

slimy salamanders (Plethodon) are a species-rich clade that diversified rap-

idly early in their evolutionary history. However, these salamander species

are distributed almost entirely allopatrically and are ecologically similar

(Kozak et al. 2006). Such clades have been termed non-adaptive radiations

(Gittenberger 1991; Kozak et al. 2006; Rundell and Price 2009). Great species

richness without substantial phenotypic disparity could arise if a clade was

predisposed to speciate in ways that do not involve adaptive divergence,

as might result from allopatric isolation in similar environments or from

the operation of sexual selection occurring in divergent ways in different

populations.

pear suddenly in some cases (e.g., colonization

of an unoccupied island) but more gradually in

others (e.g., co-radiation with another clade). We

prefer to reserve the question of timing of di-

versiﬁcation as a hypothesis to be tested among

adaptive radiations, rather than a criterion for

deciding whether a clade constitutes an adap-

tive radiation or not. At the least, if one takes the

more restrictive deﬁnition that includes timing,

then another term is needed for those clades

that produce exceptional disparity but in a non-

explosive way, perhaps such as Simpson’s (1953)

mostly forgotten “progressive occupation of

adaptive zones.”

Box 15.2 Continued

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Figure 15.04 Date 04-19-10

Species richness

Frequency

Ecological

disparity

Cordylus

lizards

Welwitschia

Plethodon

salamanders

African

cichlids

Figure 15.4 The Axes of Evolutionary Radiation Clades can be diverse in

both species richness and ecological variety, termed disparity. Clades that have

exceptional ecological disparity are adaptive radiations, whether they have great

(e.g., African lake cichlids) or little species richness (e.g., cordylid lizards). Non-

adaptive radiations are those that are exceptional in species richness, but not in

ecological disparity, such as plethodontid salamanders. Some clades are excep-

tionally non-disparate and species-poor, such as Welwitschia.

390 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 391

in any form without express written permission from the publisher.

If exceptional diversity is a key feature of adaptive

radiation, statistical methods are needed that can

test whether a radiation is exceptional. Such a

test must demonstrate that a clade contains more

disparity than would be expected under a neutral

model of diversiﬁcation, or that it is exceptionally

disparate compared to other radiations.

In principle, such questions could be ad-

dressed either by examining the fossil record or

by using phylogenetic methods. Both of these

methods have advantages and disadvantages.

Paleontological methods directly track changes

in diversity over time. By contrast, with phylo-

genetic methods using extant taxa, macroevo-

lutionary changes must be inferred. As such, re-

sults arising from these methodologies are only

as sound as their assumptions, and inadequate

models for reconstructing evolutionary history

may lead to both Type I and Type II errors in test-

ing adaptive radiation hypotheses (Revell et al.

2005; see Foote, Chapter 18). Paleontological

studies incorporate extinct taxa, and although

phylogenetic methods exist for estimating the

inﬂuence of extinction (Nee et al. 1994; Kubo

and Iwasa 1995), they often suﬀer from low

statistical power (Bokma 2009; Quental and Mar-

shall 2009; Rabosky 2009). In contrast, the phy-

logenetic approach has several distinct advan-

tages. In particular, phylogenetic studies permit

investigation of long-term evolutionary patterns

in taxa that are also well-studied ecologically—

inferences about the ecology of fossil taxa can

be unreliable, particularly when the taxa do

not have comparable extant counterparts, and

morphological homoplasy may also undermine

accurate estimation of the relationships of fossil

taxa in paleontological studies. Moreover, the

quality of the fossil record varies greatly among

taxa; phylogenetic methods can be used even

for taxa with little or no fossil record. Of course,

the most reliable insights into the large-scale

pattern of adaptive radiation will be those that

are well supported by both paleontological and

phylogenetic investigations.

Statistical approaches to the identiﬁcation

of exceptional clades have concentrated almost

entirely on patterns of lineage diversiﬁcation

rather than phenotypic diversiﬁcation. The ﬁrst

lineage diversiﬁcation models, in which specia-

tion occurred as a uniform stochastic process,

produced surprising results (Raup et al. 1973;

Slowinski and Guyer 1989). The resulting phy-

logenies tended to be topologically unbalanced,

suggesting that large diﬀerences in clade species

richness could occur by chance alone (Guyer and

Slowinski 1993; Barraclough and Nee 2001; Nee

2001, 2006). Nonetheless, many clades in the Tree

of Life are exceptionally species-rich (or species-

poor), even compared to the highly variable

neutral expectation. For instance, at a very broad

scale, Alfaro et al. (2009) identiﬁed nine such

clades among all vertebrates.

Of course, while such lineage diversiﬁcation

models are useful for testing whether species

radiations are exceptional, they do not neces-

sarily identify adaptive radiations, which are

distinguished by ecological and morphological

disparity. Paleontologists have long used mea-

sures of disparity to trace patterns of phenotypic

evolution through time, and changes in disparity

in fossil lineages have been pivotal in testing

and reﬁning adaptive radiation theory in recent

decades (Foote 1997; Roy and Foote 1997; Ciam-

paglio et al. 2001; Erwin 2001, 2007).

To date, few studies of extant taxa have at-

tempted to identify those clades that are excep-

tionally disparate using phylogenetic methods

(Losos and Miles 2002). Direct comparisons of

disparity among taxa are problematic, because

disparity is a function of the rate of evolution,

the age of a clade, and the phylogenetic topol-

ogy of the clade (O’Meara et al. 2006) (Figure 1).

One approach is to estimate the rate of pheno-

typic evolution in a phylogenetic context and to

compare rates among clades (Collar et al. 2005;

Harmon et al. 2008; Pinto et al. 2008).

Box 15.3

METHODS FOR IDENTIFYING EXCEPTIONAL CLADES

Box 15.3 Continued

Figure 1 The Effect of Phylogenetic Struc-

ture and Rate of Evolution on Expected

Disparity Under a Brownian motion model

of evolution, disparity among extant taxa is a

function of the rate of phenotypic evolution

as well as of the structure of the phylogenetic

tree relating those taxa. In (A), a phenotypic

trait evolved at a constant rate on phyloge-

netic trees that were identical in branching

order, but different in the relative timing of

divergence. In the first phylogeny, lineage

diversification was concentrated early, while

in the second phylogeny, lineage divergences

were concentrated late. Although the rate

of trait evolution was the same for each

phylogeny, greater disparity resulted when

divergences were concentrated earlier, be-

cause traits evolved independently for longer

periods of time. In (B), a trait evolved on

identical phylogenies, but the rate of evolu-

tion (σ2) differed by a factor of two between

the two phylogenies. In this case, when the

rate of evolution was higher, trait disparity

was greater. In both (A) and (B), disparity

differences are depicted graphically, using

minimum convex polygons for the evolved

trait values, and data in the upper panels are

colored to match the phylogenies and rates

under which they were generated.

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Figure Box 15.03 Date 04-19-10

–5–6 –4 –3 –2 –1 0123

–2

–3

–1

Trait 1

Trait 2

(A)

–5 –2.5 0 2.5 5–7.5 7.5

–2

–1

–3

Trait 1

σ2 = 1.0σ2 = 1.0 σ2 = 0.5σ2 = 1.0

Trait 2

(B)

392 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 393

in any form without express written permission from the publisher.

Ecological Opportunity and Adaptive Radiation

The idea that ecological opportunity is a necessary prerequisite for adap-

tive radiation dates to Simpson (1953) who argued that an ancestral species

must find itself in a setting in which “the [adaptive] zone must be occupied

by organisms for some reason competitively inferior to the entering group

or must be empty” (Simpson 1953: 207). More recently, Schluter (2000)

suggested that ecological opportunity is “loosely defined as a wealth of

evolutionarily accessible resources little used by competing taxa” (Schluter

2000: 69).

An ancestral species might find itself in the presence of ecological op-

portunity for a number of reasons:

1. colonization of isolated areas with a depauperate biota, such as

islands, lakes, or mountaintops;

2. arrival or evolution of a new type of resource;

3. occurrence in a post-mass extinction environment, again with a dep-

auperate biota;

4. evolution of a feature that provides the species with access to avail-

able resources that were previously unattainable; such a feature is

referred to as a key innovation2.

Many of the most famous examples of adaptive radiation occur on is-

lands, including such iconic radiations as Darwin’s finches, Hawaiian

honeycreepers and silverswords, and Anolis lizards. Lakes, the terrestrial

counterparts of islands, host additional renowned radiations, such as the

African Rift Lake cichlids and the many radiations in Lake Baikal. One

notable feature of many island radiations is that in the absence of many

types of organisms normally found in mainland settings, members of

the radiation have adapted in a wide variety of different ways, using re-

sources that on the mainland are utilized by taxa not present on the island

(Carlquist 1974; Leigh et al. 2007; Losos and Ricklefs 2009). The absence

of many types of predators on islands may also play a role, by allowing

organisms to use resources and habitats previously unavailable because

of predation threat (Carlquist 1974; Schluter 1988; Benkman 1991). As a

result, the ecological and phenotypic disparity of island radiations is of-

ten much greater than their mainland relatives (Carlquist 1974; Schluter

2 A key innovation is deﬁned as a trait that allows a species to interact with the

environment in a fundamentally different way (Miller 1949; Liem 1974). For

a critical discussion of the concept of key innovations, see Cracraft (1990) and

Donoghue (2005). In recent years, the term has also been used to refer to a trait

that increases the rate of species diversiﬁcation (Heard and Hauser 1995; Hodges

and Arnold 1995; Sanderson and Donoghue 1996; Ree 2005). This deﬁnition,

however, introduces a different concept; conﬂating the two under the same name

is confusing (Hunter 1998). A new term is needed for the latter phenomenon.

2000; Lovette et al. 2002; Figure 15.5). This oft-repeated phenomenon clearly

indicates the role of ecological opportunity in spurring adaptive radiation.

Species may also experience ecological opportunity without moving to

a new area if new resources appear, by immigration or evolution, where a

Darwin Bell

Sinauer Associates

Morales Studio

Figure 15.05 Date 04-19-10

Cardueline finches

Darwin’s finches

Hawaiian honeycreepers

Other passerines

–2 0 2 4

–2

Morphological trait axis I (bill width and depth)

Morphological trait axis II

(bill length)

(B)

(A)

Nectarivores

Generalists

Foragers

among leaves

Bark pickers

Seed and

fruit eaters

Figure 15.5 Adaptive Radiation of Island

Birds (A) Hawaiian honeycreepers exhibit stun-

ning morphological disparity in bill traits which

corresponds to diversity in resource use. (B) The

disparity of honeycreepers surpasses that of their

mainland relatives, the cardueline finches and

rivals that of all passerine birds. Another island

radiation, Darwin’s finches, also exhibits substan-

tial disparity. In both island radiations, species

occupy a diverse range of ecological niches uti-

lized by species in many different families on the

mainland. (A, reproduced with permission from

Pratt 2005; B, adapted from Lovette et al. 2002

and Losos and Ricklefs 2009.)

394 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 395

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clade already occurs. For example, the radiation of horses is often attributed

to the spread of grasslands in the Miocene (MacFadden 1992). Similarly, the

plant genus Espeletia has radiated extensively in paramo habitats at high el-

evations in the northern Andes (Monasterio and Sarmiento 1991; Rauscher

2002; Hooghiemstra et al. 2006). The Andes are young, and presumably, the

ancestral Espeletia rode the rising mountain chain, adapting to new high-

elevation habitats as they appeared. Hughes and Eastwood (2006) infer a

similar history for Andean Lupinus.

Ecological opportunity also appears in the aftermath of mass extinc-

tions (Erwin 2001, 2007). Surviving taxa often radiate rapidly and relatively

quickly attain similar disparity to that seen before the extinction event. In

some cases, clades radiate into parts of morphological space that previously

were unoccupied by members of that clade (Foote 1999), whereas in other

cases a surviving subclade expands its disparity to encompass parts of mor-

phological space previously occupied by other subclades that perished in

the mass extinction (Foote 1996; see Foote, Chapter 18; Ciampaglio 2002;

McGowan 2004; Friedman 2010). The high rates of phenotypic evolution

exhibited after mass extinctions by these clades strongly support the role

of ecological opportunity in spurring radiation.

The evolution of a key innovation can allow access to previously un-

attainable resources, providing the stimulus for adaptive radiation. For

example, the evolution of wings in bats allowed them to prey upon a wide

range of flying insects probably unavailable to their earthbound ancestors.

Many other examples of key innovations have been proposed, although

such hypotheses are usually difficult to test because they represent unique

historical events. One way around this difficulty is to look for putative key

innovations that have evolved multiple times to see if they have repeat-

edly led to adaptive radiation (Mitter et al. 1988; de Queiroz 2002); several

examples, such as toe pads in lizards (Russell 1979; Larson and Losos 1996),

phytophagy in insects (Mitter et al. 1988; Farrell 1998), wings in vertebrates,

and pharyngeal jaws in fish (Stiassny and Jensen 1987; Mabuchi et al. 2007),

seem to pass this test.3 However, key innovations do not necessarily lead

to adaptive radiation; the evolution of such a trait may allow the species to

interact with the environment in new ways without leading to substantial

evolutionary diversification (Fürsich and Jablonski 1984; Levinton 1988;

de Queiroz 2002).4 For example, aardvarks have evolved a suite of skeletal

3 All of these examples are cases in which taxa with the putative key innovation

exhibit substantially greater disparity than their sister taxa, although this

observation has not been statistically tested. Instead, quantitative tests in these

papers have compared species richness, rather than disparity.

4 Similarly, it is possible that the evolution of the same key innovation could lead

to radiation in some clades and not others, depending on the context in which it

evolves. Consequently, failure to ﬁnd a statistical relationship between evolution

of a putative key innovation and adaptation radiation does not indicate the

modifications permitting a termitophagous existence, but this specializa-

tion has not led to evolutionary diversification (Hunter 1998; see also Baum

and Larson 1991 on Aneides salamanders).

Although not usually discussed in these terms, the evolution of mu-

tualistic interactions may also function in a manner analogous to that of

a key innovation by providing access to resources that were previously

inaccessible (see Lane, Commentary 4). For example, the great diversity of

herbivorous insects and vertebrates would not be possible if it were not for

their mutualistic microbial gut inhabitants that allow them to digest cellu-

lose (Janson et al. 2008). Similarly, the great variety among modern corals

is likely in part the result of a mutualism between scleractinian corals and

their endosymbiotic zooxanthellae, which provides photosynthetic energy

in return for protection and nutrition (Stanley 1981).

The concept of ecological opportunity is straightforward and intuitive.

Given the number of examples in which ecological opportunity (achieved

in the four ways just enumerated) has led to adaptive radiation, there can

be little doubt that it is an important trigger to adaptive radiation. None-

theless, we may wonder whether ecological opportunity is a prerequisite

for adaptive radiation.

Can Adaptive Radiation Occur in the Absence of Pre-Existing

Ecological Opportunity?

Adaptive radiation could occur in the absence of pre-existing ecological op-

portunity either by members of a clade wresting resources away from other

taxa that had been using them or by creating their own opportunity.

COMPETITIVE REPLACEMENT OF ONE CLADE BY ANOTHER Much of the

older paleontological literature is peppered with proposals that one group

has radiated by outcompeting another, usurping its resources and forcing

it into evolutionary decline (e.g., the decline of mammal-like reptiles puta-

tively as a result of the purported superiority of dinosaurs in locomotion

or thermoregulation; Bakker 1968). However, very few of these cases hold

up to close scrutiny. Usually, when one group replaces another ecologi-

cally similar group, the explanation is that the first group went extinct, fol-

lowed by radiation of the second group (Rosenzweig and McCord 1991;

Benton 1996; Brusatte et al. 2008). In a few cases, the fossil record does

support the argument that one group has radiated at the expense of a clade

that previously utilized the same resources. Perhaps, the best example is

the interaction between cheilostome and cyclostome bryozoans, in which

cheilostomes have outcompeted cyclostomes in local interactions over the

course of many millions of years, all the while diversifying adaptively,

while cyclostomes decreased in diversity (Sepkoski et al. 2000).

evolution of the trait did not lead to adaptive radiation in any of the clades in

which it occurs (de Queiroz 2002).

396 Chapter 15 Losos • Mahler

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in any form without express written permission from the publisher.

This phenomenon of one group preventing evolutionary radiation of an-

other has been termed niche incumbency and is seen in experimental micro-

bial systems as well as in the fossil record (Brockhurst et al. 2007). It parallels

the ecological phenomenon of the priority effect, which occurs when one

species can prevent another from becoming established in a community by

dint of prior occupancy (MacArthur 1972; Chase 2007). Moreover, the obser-

vation that the introduced invasive species almost never causes the global

extinction of native species by outcompeting them5 lends support to the idea

that a radiating clade is unlikely to drive another clade to extinction through

competitive interactions (Simberloff 1981; Davis 2003; Sax et al. 2007).

CAN ADAPTIVE RADIATIONS CREATE THEIR OWN OPPORTUNITY? It would

seem, then, that ecological opportunity is usually necessary for adaptive

radiation and that in most well-studied cases, such opportunity exists prior

to adaptive radiation. However, a rarely considered alternative possibility

is that lineages create their own opportunity as they radiate. Such self-

propagation of an evolving radiation could occur in two ways.

First, as a clade radiates, the increased number of co-occurring clade

members may create opportunities for exploitation by other species. The

standard view among evolutionary biologists is that ecological opportunity

decreases through the course of a radiation as niches are filled. However,

an alternative view is that the more species that occur in a community,

the more opportunity there is for other species to take advantage of them

through predation, parasitism, mutualism, or other processes (Whittaker

1977; Tokeshi 1999; Erwin 2008). Most communities are composed of spe-

cies from many different clades, but in cases (usually on islands) in which

members of a single radiation are extremely diverse ecologically, the pos-

sibility exists for an evolutionary component to this view: as the clade radi-

ates, it may create additional opportunities, spurring further radiation, thus

creating further opportunities, and so on.

Implicit in this hypothesis is the view that interactions driving adaptive

radiation occur not only as competition for resources, but also between

species on different trophic levels. Indeed, adaptive radiations are known

in which some members of the radiation prey on other members. Among

African Rift Lake cichlids, for example, some species prey on others by eat-

ing their young, plucking their eyeballs, or rasping scales off their body.

Social parasites in hymenopterans are often closely related and are some-

times the sister taxa of the species they parasitize, which is referred to as

“Emery’s rule” (Bourke and Franks 1991; Savolainen and Vepsalainen

2003). These observations certainly indicate the possibility that adaptive

radiations create additional opportunity as they unfold. Although Schluter

5 The same is not true of introduced predators, which are responsible for scores of

species extinctions (Davis 2003; Sax et al. 2007).

(2000) suggested this idea a decade ago,6 no empirical work has addressed

this question; however, theoretical literature on the evolution of food webs

is beginning to develop (Ingram et al. 2009).

Radiations may also be self-propagating when two clades co-radiate.

Just as a clade may continually create its own ecological opportunity as it

radiates, two clades may reciprocally generate opportunity for each other

as they coevolve. Such coevolutionary radiations could take many forms.

For example, the radiation of one group, perhaps driven by interspecific

competition or predation, may create new ecological opportunities for a

second clade that utilizes members of the first as a resource. In turn, radia-

tion of the first group may continue if a species evolves some adaptation

that frees it from attack by the second group, allowing it to utilize resources

that were previously inaccessible. This last scenario is the basis of Ehrlich

and Raven’s (1964) famous escape and radiation theory of plant–herbi-

vore coevolution, and plays an important part in Vermeij’s (1987) theory

of “evolution and escalation” between predators and prey. In other cases,

co-radiations may simply result if species in one clade are each specialized

to use a single member of a second clade; in this case, adaptive radiation in

the host clade may be mirrored by radiation in their specialists. The recent

divergence of the parasitic wasp, Diachasma alloeum, in response to diver-

gence of its host, the apple maggot fly, Rhagoletis pomonella, illustrates how

such matched divergence may unfold (Forbes et al. 2009). A similar process

may have contributed to the extraordinary parallel radiations of figs and

fig wasps as well as of Glochidion trees and Epicephala moths (Herre et al.

1996; Weiblen and Bush 2002; Kato et al. 2003).

As with the role of mutualism in adaptive radiation, the processes driv-

ing coevolutionary radiations are the same as in other radiations, but the

synergistic interactions among co-radiating clades are distinctive. Such co-

evolutionary radiations may be particularly important in plant–herbivore

systems (Farrell and Mitter 1994, 1998; Roderick and Percy 2008; Winkler

and Mitter 2008; see Berenbaum and Schuler, Chapter 11).

Adaptive radiations may create their own opportunity in a second way:

members of a radiating clade may alter their environment, creating ecologi-

cal opportunities that did not previously exist. The concept of “ecosystem

engineering” refers to the role that organisms play in altering their physical

environment (Jones et al. 1994, 1997); ecosystem engineers, such as corals

or rainforest trees, change the physical environment in ways that allow the

existence of new species, potentially even leading to the evolution of eco-

logical types that otherwise would not exist (Erwin 2008). Although several

studies have documented that ecosystem engineering in one clade may

trigger adaptive radiation in another clade (e.g., corals and tetraodontiform

6 And Wilson in 1992 proposed: “what I like to call the test of a complete adaptive

radiation: the existence of a species specialized to feed on other members of its

own group, other products of the same adaptive radiation” (Wilson 1992: 118).

398 Chapter 15 Losos • Mahler

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fishes; Alfaro et al. 2007), few examples from nature document members

of an adaptive radiation altering the environment in such a way to create

ecological opportunities that have then been utilized by other members

of their own radiation. One possible example is the evolution of lobeliad

plants in Hawaii. Among the first plant clades to arrive and radiate in

this archipelago, lobeliads diversified to fill ecological roles ranging from

canopy trees to shrubs, epiphytes, and vines—one-eighth of the Hawaiian

flora in total (Givnish et al. 2009). Given their early arrival and the extent

of their ecological diversification, it is plausible that some lobeliads (e.g.,

shade-dependent shrubs) radiated in microhabitats created by other mem-

bers of the radiation (e.g., woody trees), a hypothesis that could be tested

with further phylogenetic analyses.

Laboratory studies of microbial adaptive radiation also support a role for

ecosystem engineering driving diversification. Several studies have shown

that the waste product of an ancestral microbial species created a food

source subsequently used by a second type that evolved from its ancestor

(Kassen et al. 2009).

Does “Ecological Opportunity” Have More than Heuristic Value?

The conclusion of the preceding discussion is that ecological opportunity

is usually necessary for adaptive radiation, but whether we can predict a

priori if a clade will radiate is not clear for two reasons. First, ecological

opportunity, though usually necessary, may not be sufficient for radia-

tion. Second, ecological opportunity may be extremely difficult to define

objectively a priori and, as a result, the concept may have limited utility for

predicting when clades would be expected to radiate adaptively, as op-

posed to explaining retrospectively why they did so.

Many clades fail to radiate despite apparently abundant ecological op-

portunity. For example, the Galápagos and Hawaii are famous for their bird

radiations (finches and honeycreepers, respectively), but many other bird

lineages on these islands have failed to produce adaptive radiations, in-

cluding mockingbirds on the Galápagos (Arbogast et al. 2006) and thrushes

on Hawaii (Lovette et al. 2002). The same is true of many other island taxa.

Radiation may not occur in such circumstances for several reasons:

1. The perception of ecological opportunity may be mistaken.

2. Inability to access or utilize resources (e.g., from the lack of genetic

variation or phenotypic plasticity that could produce phenotypes

capable of taking advantage of novel available resources).

3. Lack of speciation: if, for some reason, speciation cannot occur (as dis-

cussed subsequently), then adaptive radiation cannot result.

4. Inability to diversify ecologically : even when speciation can occur,

if the resulting descendant species are unable to diverge phenotypi-

cally to specialize on different resources, then a clade may not be able

to radiate adaptively. Lack of such evolvability (Liem 1974; Vermeij

1974; Cheverud 1996; Wagner and Altenberg 1996; Gerhart and

Kirschner 1998; Rutherford and Lindquist 1998; see G. Wagner, Chap-

ter 8) may occur for a variety of reasons, often referred to as “evolu-

tionary constraints” (see Wray, Chapter 9).

The first hypothesis that one might pose about a clade that has failed to

radiate could invoke lack of ecological opportunity, but it is not clear how

one would test this idea.7 A way of doing so might involve estimating selec-

tion on an adaptive landscape (Fear and Price 1998; Schluter 2000; Arnold

et al. 2001). The existence of unutilized adaptive peaks might suggest that a

species had the opportunity to diversify and occupy those peaks. Of course,

the existence of multiple adaptive peaks on a landscape does not guarantee

that selection would push a clade to diversify to produce species occupy-

ing all of these peaks: speciation must occur, and the landscape itself will

change when other species are present. Research of this type has rarely been

conducted, the most thorough being studies on Darwin’s finches (Schluter

and Grant 1984; Schluter 2000; see also Case 1979). Development of these

sorts of ideas is needed to make ecological opportunity a fully operational

and predictive concept.

As a result, currently ecological opportunity is only recognizable after the

fact, as a plausible and often surely correct explanation for why a clade radi-

ated.8 As such, the concept may have great heuristic value in understanding

what causes adaptive radiation, but it may have little operational value in

the absence of a radiation to predict whether radiation could occur.

Adaptive Divergence, Speciation, and Adaptive Radiation

Adaptive radiation has two components: proliferation of species (specia-

tion) and divergence of species into different ecological niches (Losos 2009;

see Harrison, Chapter 13). Two important questions concern: (1) whether

any process other than natural selection could produce adaptive divergence

and (2) whether speciation and adaptation are causally connected.

Divergence of species to utilize different aspects of the environment could

occur in two ways, either with genetic drift playing a large role or by diver-

gent natural selection. Although drift by itself would not be expected to lead

7 In this regard, one might suggest that the concept of ecological opportunity

suffers from the same problems as the empty niche concept (Chase and Leibold

2003). Both empty niches and ecological opportunity are difﬁcult to identify in

the absence of species that ﬁll or take advantage of them. Moreover, one might

question whether resources are ever truly unutilized. How often, for example, is

some type of food resource not eaten by any organism? If nothing else, they are a

resource for decomposers, which is the reason for the wording of the deﬁnitions

of ecological opportunity presented earlier.

8 Ecological opportunity is also an explanation for why some species exhibit

exceptionally broad ecological and phenotypic diversity, which is arguably the

ﬁrst step in adaptive radiation (Parent and Crespi 2009).

400 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 401

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to adaptive change, in an adaptive landscape, it is possible that it could move

a population off one adaptive peak and into the domain of another (the basis

of Wright’s 1932 famous shifting balance theory). Alternatively, drift could

move a population along an adaptive ridge, from one high point in an adap-

tive landscape to another equally high point, assuming that the two points

are connected by a ridge of equally high fitness (Schluter 2000). While these

scenarios could ultimately result in the evolution of a suite of adaptively

differentiated species, they have received relatively little empirical support.

Rather, the standard and widely accepted view is that adaptive radiation

is driven by divergent natural selection, in which species diverge as they

adapt to use different parts of the environment. Most theories of adap-

tive radiation assume that a trade-off exists, such that enhanced adapta-

tion to use one part of the environment comes with a concomitant cost

of decreased adaptation to another part of the environment. Evidence for

such trade-offs is strongly implied by work on polymorphisms and local

adaptation (Schluter 2000), although the specific traits involved are often

unknown (see Agrawal et al., Chapter 10).

With regard to the second question, speciation and adaptive divergence

could be related in a number of ways:

1. Allopatric speciation could occur with adaptive divergence.

2. Allopatric speciation could occur without adaptive divergence, fol-

lowed by adaptive divergence when species secondarily establish

sympatry.

3. Some degree of adaptive divergence and evolution of reproductive

isolation could occur in allopatry, followed by enhanced adaptive

divergence and completion of the speciation process in sympatry (if

not completed in allopatry).

4. Speciation could occur in sympatry accompanied by adaptive diver-

gence. With respect to adaptive radiation, adaptive divergence is usu-

ally invoked as an integral part of the speciation process, though in

theory, sympatric speciation could occur in non-adaptive ways (e.g.,

by polyploidy), followed by adaptive divergence, which would occur

as in the first scenario in this list.

Few workers have suggested that most or all of the adaptive divergence

during adaptive radiation evolves in allopatry (option 1). Rather, sympatric

divergence, either during or after speciation (options 2, 3, and 4), is the pri-

mary, though not exclusive, focus of theoretical and empirical discussion.

Sympatric speciation driven by disruptive selection is in a way the most

biogeographically parsimonious explanation for the occurrence of a clade of

co-occurring, ecologically differentiated species, because it does not require

the invocation of one or more rounds of range contraction and expansion to

permit allopatric speciation followed by current-day sympatry. Nonethe-

less, the possibility of sympatric speciation of this sort is highly controver-

sial, and probably the majority of workers consider the prerequisites for

it to occur to be very stringent and likely to be met by few organisms in

most settings (Coyne and Orr 2004; Gavrilets 2004; Bolnick and Fitzpatrick

2007; see Harrison, Chapter 13). In a few examples, the case for adaptive

radiation by sympatric speciation is strong. The most convincing is the

occurrence of two clades of ecologically differentiated cichlid fishes, each

one in different volcanic crater lakes in Cameroon (Schliewen et al. 1994).

The monophyly of the clades (comprised of 9 and 11 species) makes in situ

speciation far more plausible than the alternative of many colonization

events followed by extinction of related forms outside the lakes (which

would make the lake species monophyletic with respect to extant species).

The lakes are small and homogeneous, so it is hard to imagine an allopatric

phase in the speciation process, leading to the conclusion that sympatric

speciation likely occurred.

Many clades of insects, some extremely species-rich, are composed of

species adapted to specialize on different host plants (see Berenbaum and

Schuler, Chapter 11). In many cases, multiple—sometimes many—clade

members occur sympatrically. Some workers in this area consider the evo-

lution of sympatric host-specialist species to be most readily explicable

by sympatric speciation (Berlocher and Feder 2002; Drès and Mallet 2002;

Abrahamson and Blair 2008). However, controversy over the theoretical

likelihood of sympatric speciation also pertains to host race speciation

(Coyne and Orr 2004; Gavrilets 2004; Bolnick and Fitzpatrick 2007). Fu-

tuyma (2008) argued that the empirical evidence in support of this view is

not generally strong and suggests that host shifts in allopatry are a likely

alternative possibility. Although the literature on these insects usually is

not couched in terms of adaptive radiation (exceptions include Després

and Cherif 2004; Price 2008; Roderick and Percy 2008), many host-specialist

complexes surely are adaptive radiations, and if sympatric speciation is

a common mode of speciation in these groups, then they may represent

examples of adaptive radiation by sympatric speciation.

The extreme alternative to adaptive divergence during sympatric specia-

tion is speciation in allopatry without adaptive ecological divergence. Sub-

sequently, the new species become sympatric and as a result of divergent

natural selection, adapt to different ecological niches (i.e., ecological char-

acter displacement). Speciation without adaptive divergence could occur

if allopatric populations diverge and become reproductively isolated as a

result of genetic drift or if sexual selection pressures in the two popula-

tions lead to the evolution of different mating preferences (Gittenberger

1991; Price 2008). One difficulty with these scenarios is that, if resources

are limiting, ecologically undifferentiated species may compete when they

become sympatric and thus, may not be able to coexist long enough for evo-

lutionary divergence to occur (MacArthur and Levins 1967; Slatkin 1980;

Gomulkiewicz and Holt 1995).

An intermediate possibility emphasizes the role that different selec-

tive environments may play in causing allopatric populations to diverge.

Studies in both the laboratory and in nature clearly indicate that isolated

402 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 403

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populations experiencing different selective pressures are more likely to

evolve reproductive isolation as an incidental result of adaptive differentia-

tion (Rice and Hostert 1993; Funk et al. 2006; Funk and Nosil 2008) (Figure

15.6). Consequently, speciation is more likely to occur, or at least be initiated,

by populations experiencing different selective pressures. Moreover, if such

populations become sympatric, the evolved differences in ecology increase

the possibility that the populations can coexist long enough for character

displacement to occur, leading to greatly enhanced ecological differentia-

tion that permits coexistence. This scenario corresponds to the archipelago

model of adaptive radiation (Grant and Grant 2008a; Price 2008).

Because species proliferation is required for adaptive radiation to occur,

taxa that are more likely to speciate may also be more likely to adaptively

radiate. Thus, factors that predispose taxa to speciate, such as a mating

system emphasizing female choice, may be linked to adaptive diversifica-

tion (Schluter 2000; Rundell and Price 2009). In the same vein, the evolu-

tion of a trait that leads to enhanced speciation rates may be the trigger

that promotes adaptive radiation in a group, if ecological opportunity is

already present.

Overall, the role of speciation in adaptive radiation is poorly under-

stood. In recent years, “ecological speciation”—the idea that divergent ad-

aptation to different environments leads to the speciation—has attracted

considerable attention (for insightful reviews, see Hendry 2009 and see

Harrison, Chapter 13). There is no doubt that adaptation to different en-

vironments by allopatric populations enhances the likelihood that those

populations will become reproductively isolated, and this model is a key

stage in the standard model for adaptive radiation on islands. Whether or

not ecological speciation in sympatry (i.e., sympatric speciation) commonly

occurs and leads to adaptive radiation is an open question. Similarly, the

role of nonadaptive modes of speciation, such as founder effect speciation,

in adaptive radiation is also controversial (Coyne and Orr 2004; Gavrilets

2004; Futuyma 2005; Price 2008). More generally, the extent to which adap-

tive radiation is limited by the production of new species is unclear and

thus the degree to which factors that promote speciation may be important

indirect promoters of adaptation radiation remains uncertain.

Adaptation to Different Aspects of the Environment in the Absence

of Interspecific Interactions

Regardless of how speciation occurs, what ecological mechanisms drive

adaptive divergence? Divergent natural selection is the underlying cause,

but the question is whether the driving force behind such selection is sim-

ply adaptation to different aspects of the environment or whether inter-

specific interactions change the selective landscape, producing divergent

selection that would not occur in the absence of the interacting species

(Schluter 2000).9

It is easy to envision how two allopatric populations experiencing differ-

ent environments would evolve different adaptations. Moreover, because the

environment and hence, the adaptive landscape is rarely identical in different

places, it is possible that two adaptive peaks that are separated by an adap-

tive valley in one location may be connected by an adaptive ridge in another.

Suppose a population on one island occupied the lower of two adaptive

peaks, which were separated by an adaptive valley, so that the higher peak

was not attainable. If members of that population colonized a second island

on which the peaks were connected by an adaptive ridge, then the popula-

tion would adapt to the higher peak. Subsequently, if members of the second

population colonized the first island, they would occur on the higher peak,

producing sympatry of the species on different peaks (Figure 15.7).

In theory, this sort of scenario, in which adaptive divergence occurs

entirely in allopatry, could lead to adaptive radiation, producing species

adapted to many different aspects of the environment. Most views of adap-

tive radiation do not take such an extreme view, though proponents of

the role of interspecific interactions envision allopatric differentiation as

the initial step in divergence, setting the stage for subsequent, much more

substantial divergence in sympatry that is driven by sympatric interactions

(i.e., character displacement).

An alternative view is that divergent selection in sympatry can split an

initially homogeneous population into distinct, reproductively isolated and

9 In this discussion, we consider the food an organism eats to be part of the

environment. By interspeciﬁc interactions, we refer to interactions among species

on the same trophic level or between the focal species and other species on

higher trophic levels.

Darwin Bell

Sinauer Associates

Morales Studio

Figure 15.06 Date 04-21-10

0.0 0.25 0.5 0.75

r = +0.43

1.0

Habitat divergence

Residual postmating isolation

Figure 15.6 The Relationship between Divergent Adaptation and

Reproductive Isolation The more dissimilar two species are in habitat use, the

greater the degree of reproductive isolation that has evolved between them.

Each point represents the degree of difference between two closely related spe-

cies or populations. (Adapted from Funk et al. 2006.)

404 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 405

in any form without express written permission from the publisher.

adaptively differentiated populations. Some variants of this model envision

intraspecific resource competition or interspecific interactions as the driv-

ing force, but many prominent proposals, particularly those concerning

host–plant specialists (see following discussion), simply invoke adaptation

to different aspects of the environment, requiring a tradeoff such that dis-

ruptive selection produces a bimodal distribution of phenotypes. As just

discussed, the prerequisites for reproductive isolation to evolve in such a

scenario are very strict, and controversy still exists on how likely it is to

occur, even in host–plant specialized insects.

Adaptation to Different Aspects of the Environment

as a Result of Interspecific Interactions

Interspecific Competition

Dating back to the seminal work by Simpson (1953), which focused pri-

marily on vertebrates, a commonly held view is that adaptive radiation

primarily results from interspecific competition for resources, leading to

character displacement and adaptation to different resources (Schluter

2000; Grant and Grant 2008a). Repeated numerous times, this process leads

to sympatric coexistence of species adapted to a variety of different ecologi-

cal niches (i.e., an adaptive radiation).

Although character displacement was controversial in the 1970s and

1980s, a growing consensus exists that it is an important evolutionary phe-

nomenon (Schluter 2000; Dayan and Simberloff 2005; Pfennig and Pfennig

2009). Experimental studies have confirmed that interspecific competition

can lead to strong divergent selection (Schluter 1994; Schluter 2003), and the

process of character displacement has been directly observed in the field in

Darwin’s finches (Grant and Grant 2006) (Figure 15.8) as well as in labora-

tory studies (e.g., Barrett and Bell 2006; Tyerman et al. 2008; Kassen 2009).

It seems safe to conclude that interspecific competition-driven character

displacement is a common means by which adaptive radiation occurs.

The question is, then, whether interactions other than competition can

lead to adaptive radiation, and if so, whether they have been important in

driving adaptive radiations throughout the history of life.

Predation, Parasitism, and Herbivory

In ecological terms, predation, parasitism, and herbivory are similar pro-

cesses in that they refer to individuals of one species directly consuming

members of another species (hence, we refer to all as “predators” in the

following discussion). These processes could produce divergent natural se-

lection pressures when species adapt to different predators or when species

adapt in divergent ways to the same predator. Moreover, species initially

preyed upon by the same predator may diverge so as not to share the same

predator. Although predation may spur divergence and diversification, it

also can hinder it, and the extent to which predation plays an important

role in driving adaptive radiation remains poorly understood (Vamosi

2005; Langerhans 2006).

One can easily envision how species occurring in different places, with

different predation regimes, would face selection to evolve different pheno-

types. Several recent studies have demonstrated the importance of preda-

tion in driving such divergence. For example, both mosquitofish and dam-

selflies exhibit differences in their behavior, habitat use, and morphology

depending on which predators are present in the lakes in which they occur

(McPeek et al. 1996; Stoks et al. 2003; Langerhans et al. 2007).

In sympatry, predation-driven selection may be divergent for several

reasons. First, multiple ways may exist to avoid predation. For example,

Timema walking sticks that use different host plants have diverged to en-

hance crypsis on the differently colored plants; manipulative experimental

studies demonstrate that selection is divergent when predators are pres-

ent (Nosil and Crespi 2006) (Figure 15.9). Among garter snakes, disruptive

selection favors striped individuals that rapidly flee from predators and

Darwin Bell

Sinauer Associates

Morales Studio

Figure 15.07 Date 04-29-10

Mean

fitness

Island A

Mean

fitness

Island B

(A)

(B)

Colonization

Backcolonization

Trait 2

Trait 1

Figure 15.7 Peak Shifts along an Adaptive Ridge (A) The ancestral species

occurs on the lower adaptive peak on Island A. Because an adaptive valley lies

between the two peaks, natural selection cannot drive the population to the sec-

ond peak. (B) However, on Island B, an adaptive ridge connects the ancestral posi-

tion to a higher peak, and when individuals immigrate to Island B from Island

A, the new population on Island B evolves a new morphology. Subsequently, the

population on Island B evolves reproductive isolation. When individuals from

Island B then recolonize Island A, they may evolve to the second peak on that

island, leading to the coexistence of two species—one on each adaptive peak.

(Adapted from Schluter 2000.)

406 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 407

in any form without express written permission from the publisher.

blotched individuals that remain hidden (Brodie 1992). In

theory, species evolving different anti-predator adapta-

tions might not differ in any other way with regard to re-

source or habitat use, in which case ecological opportunity

might not be involved in adaptive divergence. However,

most documented examples include correlated shifts in other ecological and

behavioral aspects; the evolution of body armor, for example, has conse-

quences for locomotion, which in turn may affect where and how an animal

can forage (Bergstrom 2002; Losos et al. 2002). Consequently, in this pred-

ator-driven scenario for adaptive radiation, ecological opportunity would

still be required; multiple distinct habitats or resources to which different

prey species could adapt would be necessary, and these different niches

could not already be preempted by other species.

Selection may also favor sympatric species to diverge in habitat use so

as to avoid being preyed upon by the same predator. If prey species are

preyed upon by the same predator, then under some circumstances, in-

creased population size of one of the prey species would lead to increased

population size of the predator; thus, the population size of the other prey

species would decrease, as they are preyed upon by the greater number of

predators. The result is that a negative relationship would exist between the

population sizes of the prey species, just as would occur through interspe-

cific competition (Holt 1977). Assuming the predator species is not able to

function equally successfully in all parts of the environment, prey species

may diverge to use different resources or habitats, if they are available, and

thus no longer share predators. Subsequently, prey species would adapt to

the different habitats or resources they were utilizing, producing the same

outcome as competition-driven character displacement: an adaptive radia-

tion driven by “competition for enemy free space” (Jeffries and Lawton

1984) or “apparent competition” (Holt 1977).

In theory, adaptive radiation also could result from predation-driven di-

vergent selection by the means just outlined. However, we are aware of few

purported cases. The diversity of some tropical butterfly clades, involving

multiple mimicry complexes and a suite of other ecological and behavioral

differences, might be one example (Elias et al. 2008).

Processes Driving Radiation: Conclusions

The role of interspecific competition in driving evolutionary radiation is

well established and likely to be of paramount importance. Other ecologi-

cal processes may be important, either directly (e.g., predation, herbivory,

Darwin Bell

Sinauer Associates

Morales Studio

Figure 15.08 Date 04-19-10

(A)

(C)

7 8 9 10 11 12 13 14 15 16 17 18 19

Beak depth (mm)

Individuals

G. fortis G. magnirostris

(a)

(b)

1975 1980 1985 1990 1995 2000 2005

–1.0

–1.5

–0.5

0.0

0.5

1.0

Year

Beak size

(B)

Figure 15.8 Character Displacement in Darwin’s Finches (A) Daphne Major, in

the Galápagos Islands, harbors both the large ground finch, Geospiza magnirostris

(A2), and the medium ground finch, Geospiza fortis (A1, A3), the latter of which

exhibits substantial variability in beak shape. Only large-beaked birds can eat

large seeds, such as those from Tribulus cistoides (A4). (B) During the drought

of 1977, when only the medium ground finch occurred on the island, small

seeds were rapidly consumed and only large seeds remained. Selection strongly

favored large-beaked medium ground finches (as indicated by the calculation

of selection gradients, which are not shown here), and the population evolved

larger beak size. Another drought occurred in 2003 and 2004; however, in the

intervening years, the large ground finch had colonized Daphne Major. During

this drought, the large ground finches monopolized the larger seeds. Mortality

was very high in both species, and in the medium ground finch, smaller-beaked

birds that could eat the few remaining small seeds were favored, and the popula-

tion evolved smaller beak size, the opposite of what occurred in the absence of

the large-beaked ground finch. Beak size units represent scores on the first axis of

a principal components analysis of six bill measurements. (C) Thus, in the 2003–

2004 drought, selection favored smaller-beaked birds in the medium ground finch

and larger-beaked birds in the large ground finch, and the phenotypic distribu-

tions before the drought (indicated by blue bars) and afterwards (indicated by red

bars) can be compared; as a result, differences in beak size between the two spe-

cies were greater after the drought (arrow a) than before (arrow b), making this a

classic example of character displacement. (A, photos from Grant and Grant 2006;

B, adapted from Grant and Grant 2006; C, adapted from Grant and Grant 2008b.)

408 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 409

in any form without express written permission from the publisher.

and parasitism) or indirectly (e.g., mutualism and coevolution), by creat-

ing the opportunity for other processes to operate. However, empirical

evidence demonstrating the role of other ecological processes is sparse. To

some extent, this paucity of case studies, may be a result of the historical

focus on competition as a driver of character displacement, but attention

among both theorists and ecologists to other mechanisms has occurred

for long enough now that one might expect more examples to have been

documented. The lack of such examples would seem to be indicative of

their limited importance relative to that of direct competition. Certainly,

the evolution of mutualisms and coevolution are events that can trigger

adaptive radiation. How frequently they occur is unclear.

Laboratory experiments on microbial evolution support these conclu-

sions (see Dykhuizen, Commentary 2). Kassen (2009) reviewed the rapidly

growing literature in this field and found overwhelming support for the role

of interspecific competition as the primary driver of adaptive radiation. The

addition of predators as an experimental treatment occasionally enhanced

adaptive radiation but only when the variety of resources was limited.

In situations with a wide variety of resources, the presence of predators

slowed, rather than enhanced, the rate of adaptive diversification (Meyer

and Kassen 2007; see also Benmayor et al. 2008). Other possible triggers

for adaptive radiation, such as ecosystem engineering or the evolution of

mutualisms, also rarely are important (Kassen 2009). The correspondence

between the results from experimental laboratory studies and the empirical

literature from nature suggests that interspecific competition is the primary

driver of adaptive radiation.

Conclusions and Future Directions

Many of what we consider the classic ideas about adaptive radiation are

well supported. In particular, ecological opportunity usually is the key

to adaptive radiation, and interspecific competition often is the driving

force behind it. Nonetheless, these are generalizations, and further work

is needed to understand the relative frequency and significance of alterna-

tives. In many cases, other possibilities, such as the role of predation in

driving adaptive radiation or the extent to which radiations create their

own ecological opportunity, have been little explored. Whether further

work will alter the bigger picture of our understanding of adaptive radia-

tion remains to be seen.

We also conclude that while ecological opportunity is typically necessary,

it is not sufficient for adaptive radiation, as many clades seemingly in the

presence of opportunity fail to radiate. Several factors likely contribute, but

at present, these are too poorly understood to predict with any certainty

whether adaptive radiation will occur in the presence of ecological opportu-

nity. Why, for example, did Darwin’s finches, but not mockingbirds, radiate

in the Galápagos? Experimental diversification studies have come to the fore-

front in filling this gap; the combination of replication, strict environmental

control, and fine-scale genetic characterization of lineages makes for a prom-

ising approach to dissect the nature of historical contingency in adaptive ra-

diation (Lenski and Travisano 1994; Fukami et al. 2007; Blount et al. 2008).

While we have offered a review of the current knowledge pertaining

to adaptive radiation, numerous basic questions about adaptive radiation

remain unanswered, and recent conceptual and technological advances

promise to lead adaptive radiation research into exciting new directions.

Toward this end, we suggest that new approaches that take advantage of

both conceptual and technological advances may be instrumental in mov-

ing forward understanding of adaptive radiation in years to come.

Darwin Bell

Sinauer Associates

Morales Studio

Figure 15.09 Date 04-21-10

0.0–4.0 –4.04.0

0.10

0.30

0.50

0.70

Brightness contrast

Fitness

(A) Ceanothus: predation present

0.0 4.0

Brightness contrast

(B) Adenostoma: predation present

0.0–4.0 4.0

0.10

0.30

0.50

0.70

Brightness contrast

Fitness

0.0–4.0 4.0

Brightness contrast

(D) Adenostoma: predation absent

Figure 15.9 Selection for Background Matching in the Walking Stick, Timema

cristinae Experimental studies of selection reveal that in the presence of avian

predators, dull stripes, and bright bodies (“brightness contrast” is body bright-

ness minus stripe brightness) are favored in the Ceanothus ecotype (A) and

bright stripes and dull bodies in the Adenostoma ecotype (B). In the absence of

predators, selection does not differ between insects on the two bushes (C and D).

(Adapted from Nosil and Crespi 2006.)

410 Chapter 15 Losos • Mahler

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Adaptive Radiation: The Interaction of Ecological Opportunity, Adaptation, and Speciation 411

in any form without express written permission from the publisher.

Our review has focused, for the most part, on the role of external envi-

ronmental factors in shaping adaptive radiation. However, over the last

several decades, evolutionary biologists have debated the role that internal

constraints—manifested in limitations and directionality in the availability

of phenotypic variation upon which selection can operate—play in limiting

and directing evolutionary change (Gould 2002).

The role of such constraints on adaptive radiation is now being addressed

in two distinctive ways. On one hand, a number of researchers have sug-

gested that interspecific hybridization can provide enhanced variation that

may be critical in allowing extensive adaptive diversification. On the other

hand, the burgeoning field of genomics is now at last permitting evolution-

ary biologists to truly understand the relationship between genetic change

and phenotypic response.

Hybridization

Several authors have recently suggested that hybridization among closely

related species may play an important role in generating adaptive diversity

during the early stages of adaptive radiation (Rieseberg et al. 1999; See-

hausen 2004; Grant and Grant 2008a,b; Mallet 2009). Increasingly sophis-

ticated methods are being developed to distinguish past gene flow from

incomplete lineage sorting, permitting detection of historical hybridiza-

tion in a phylogenetic framework (Hey and Nielsen 2004; Hey et al. 2004;

Kubatko 2009), which may facilitate investigation of the contribution of

hybridization to adaptive diversification. Nonetheless, directly measuring

the effect of hybridization on divergence in the wild is often difficult be-

cause of the low frequency of hybridization events and the infeasibility of

tracking hybrid lineages over many generations, although Grant and Grant

(2008b, 2009) provide remarkable examples in Darwin’s finches. However,

future studies might assess the role of hybridization in adaptive radiation

by testing whether radiations that exhibit historical signatures of hybrid-

ization exhibit greater adaptive diversity than radiations in which there is

little evidence of hybridization.

Genomics

Thanks to the ever-decreasing cost of genome sequencing, the ability to

examine the genomes of multiple members of an adaptive radiation will

soon be readily available. With such information, researchers will be able

to examine the extent to which genetic architecture constrains and directs

the pathways by which adaptive diversification has occurred. Combined

with studies of natural selection in the field, we soon will have the ability

to fully integrate genetics and the study of natural selection to understand

how and why adaptive radiation has occurred. Experimental studies of this

sort have already been conducted (e.g., microbial laboratory experiments:

Bantinaki et al. 2007 and Spencer et al. 2007; sticklebacks: Barrett et al. 2008)

and no doubt will soon become commonplace. The next 10–20 years should

prove extremely enlightening as the integration of genomic and selection

studies, in a phylogenetic context, ushers in a golden age for the study of

adaptive radiation.

The Impact of Adaptive Radiation on Communities and Ecosystems

Finally, virtually all research on adaptive radiation has investigated the in-

fluence of ecological factors on adaptive diversification, but until recently,

few have asked how the process of adaptive radiation may alter the struc-

ture of communities and ecosystems. Adaptive radiation typically involves

a dramatic change in the ecological diversity of a lineage, usually within a

local setting. Diversification may influence community interactions, alter

food webs, and ultimately affect nutrient and energy flow in ecosystems,

and radiations have been implicated in major ecological changes in Earth’s

history (e.g., the rise and proliferation of autotrophs changing the atmo-

spheric oxygen concentration roughly 2 billion years ago). However, only

recently has research specifically sought to quantify the influence of evo-

lutionary diversification on community structure and ecosystem function

(Loueille and Loreau 2005, 2006; Harmon et al. 2009; Ingram et al. 2009).

Continued research in this direction may result in a richer understanding

of the complex and interactive relationship between ecological and evolu-

tionary diversity.

Acknowledgments

This chapter benefited from discussions with and critiques by: Adam Al-

gar, Mike Bell, Joel Cracraft, Doug Futuyma, Luke Harmon, Mark McPeek,

Trevor Price, Bob Ricklefs, John Thompson, and Peter Wainwright.

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Aug 2023
MOL PHYLOGENET EVOL

African-Malagasy species of the bat genus Miniopterus are notable both for the dramatic increase in the number of newly recognized species over the last 15 years, as well as for the profusion of new taxa from Madagascar and the neighboring Comoros. Since 2007, seven new Malagasy Miniopterus species have been described compared to only two new species since 1936 from the Afrotropics. The conservative morphology of Miniopterus and limited geographic sampling in continental Africa have undoubtedly contributed to the deficit of continental species. In addition to uncertainty over species limits, phylogenetic relationships of Miniopterus remain mostly unresolved, particularly at deeper backbone nodes. Previous phylogenetic studies were based on limited taxon sampling and/ or limited genetic sampling involving no more than five loci. Here, we conduct the first phylogenomic study of the Afrotropical Miniopteridae by analyzing up to 3772 genome-wide ultraconserved elements (UCEs) from historic and modern samples of 70 individuals from 25 Miniopterus species/lineages. We analyze multiple datasets of varying degrees of completeness (70, 90, and 100 percent complete) using partitioned concatenated maximum likelihood and multispecies coalescent methods. Our well-supported, species-level phylogenies resolved most (6/8 or 7/8) backbone nodes and strongly support for the first time the monophyly of the Malagasy radiation. We inferred the crown age of African Miniopteridae in the late Miocene (10.4 Ma), while the main lineages of Miniopterus appear to have contemporaneously diversified in two sister radiations in the Afrotropics and Madagascar. Species-level divergence of 23 of 25 African + Malagasy Miniopterus were estimated to have 95 % HPDs that overlap with the late Miocene (5.3-10.4 Ma). We present ancestral range estimates that unambiguously support a continental African radiation that originated in the Zambezian and Somalian/Ethiopian biogeographic regions, but we cannot rule out back colonization of Africa from Madagascar. The phylogeny indicates genetic support for up to seven new species.

Reappraising the evolutionary history of the largest known gecko, the presumably extinct Hoplodactylus delcourti, via high-throughput sequencing of archival DNA

Article

Full-text available

Jun 2023

Hoplodactylus delcourti is a presumably extinct species of diplodactylid gecko known only from a single specimen of unknown provenance. It is by far the largest known gekkotan, approximately 50% longer than the next largest-known species. It has been considered a member of the New Zealand endemic genus Hoplodactylus based on external morphological features including shared toe pad structure. We obtained DNA from a bone sample of the only known specimen to generate high-throughput sequence data suitable for phylogenetic analysis of its evolutionary history. Complementary sequence data were obtained from a broad sample of diplodactylid geckos. Our results indicate that the species is not most closely related to extant Hoplodactylus or any other New Zealand gecko. Instead, it is a member of a clade whose living species are endemic to New Caledonia. Phylogenetic comparative analyses indicate that the New Caledonian diplodactylid clade has evolved significantly more disparate body sizes than either the Australian or New Zealand clades. Toe pad structure has changed repeatedly across diplodactylids, including multiple times in the New Caledonia clade, partially explaining the convergence in form between H. delcourti and New Zealand Hoplodactylus. Based on the phylogenetic results, we place H. delcourti in a new genus.

Diseño de juegos y las inteligencias biológicas, computacional y humana: mapeando relaciones

Article

Apr 2024

En la última década, el campo del diseño de juegos ha experimentado diversas iteraciones con una amplia gama de áreas.

Divergent Evolution

Chapter

May 2022

Pallavi Gautam

From Fossils to Living Canids: Two Contrasting Perspectives on Biogeographic Diversification

Preprint

Full-text available

Sep 2023

The Canidae are an ecologically important group of dog-like carnivores that arose in North America and spread across the planet around 10 million years ago. The current distribution patterns of species, coupled with their phylogenetic structure, suggest that Canidae diversification may have occurred at varying rates across different biogeographic areas. However, such extant-only analyses undervalued the rich fossil history of the group because of a limitation in methods development. Current State-dependent Speciation and Extinction (SSE) models are (i) often parameter-rich which hinders reliable application to relatively small clades such as the Caninae (the only extant subclade of the Canidae consisting of 36 extant species); and (ii) often assume as possible states only the states that extant species present. Here we extend the SSE method SecSSE to apply to phylogenies with extinct species as well (111 Caninae species) and compare the results to those of analyses with the extant-species-only phylogeny. The results on the extant-species tree suggest that distinct diversification patterns are related to geographic areas, but the results on the complete tree do not support this conclusion. Furthermore, our extant-species analysis yielded an unrealistically low estimate of the extinction rate. These contrasting findings suggest that information from extinct species is different from information from extant species. A possible explanation for our results is that extinct species may have characteristics (causing their extinction), which may be different from the characteristics of extant species that caused them to be extant. Hence, we conclude that differences in biogeographic areas probably did not contribute much to the variation in diversification rates in Caninae.

Climatic variation along the distributional range in Cuban Anolis lizards: Species and ecomorphs under future scenarios of climate change

Article

Full-text available

Feb 2023

Geographical ranges and physiological tolerances of species are correlated, and it can be expected that widespread species encounter higher climatic variation across their distributions than restricted species. Widespread species should consequently be more tolerant to extreme or variable weather conditions, and may have the ability to better conserve their current geographical ranges under future climate change scenarios. We tested this hypothesis by studying the relationship between the climatic variation experienced by restricted and widespread Anolis lizards from different ecomorphs and regions of Cuba and the distributional shifts induced by climate change. We selected seven bioclimatic variables from WorldClim to characterize the realized climatic niche of 12 Cuban anoles, where the coefficients of variation of each variable were taken as a measure of climatic variation. We used niche modeling to predict changes in suitable habitats under future climatic scenarios. We found that species from Eastern Cuba occupy areas with the highest climatic variation, likely related to the topography of the region. Crown giant anoles experienced habitats with lower climatic variation in comparison with species from other ecomorphs, which together with their tree canopy habitat and large body size may represent a disadvantage to face changing climates. All species will experience a severe decrease in their habitat suitability, with the Western species being predicted to lose a higher proportion of suitable habitat. Combining niche modeling with physiological data would better predict the effects of climate change on Cuban lizards and might allow taking management actions for species and habitats to mitigate the possible negative impacts of this phenomenon.

Rapid speciation, hybridization and adaptive radiation in the Heliconius melpomene group

Chapter

Full-text available

Jan 2001

James Mallet

Bringing together the viewpoints of leading ecologists concerned with the processes that generate patterns of diversity, and evolutionary biologists who focus on mechanisms of speciation, this book opens up discussion in order to broaden understanding of how speciation affects patterns of biological diversity, especially the uneven distribution of diversity across time, space and taxa studied by macroecologists. The contributors discuss questions such as: Are species equivalent units, providing meaningful measures of diversity? To what extent do mechanisms of speciation affect the functional nature and distribution of species diversity? How can speciation rates be measured using molecular phylogenies or data from the fossil record? What are the factors that explain variation in rates? Written for graduate students and academic researchers, the book promotes a more complete understanding of the interaction between mechanisms and rates of speciation and these patterns in biological diversity.

How and Why Species Multiply: The Radiation of Darwin's Finches

Book

Mar 2020

Butterflies and plants: a study in coevolution

Article

Dec 1964
EVOLUTION

WHEN DOES EVOLUTION BY NATURAL SELECTION PREVENT EXTINCTION?

Article

Feb 1995
EVOLUTION

INFERRING THE RATES OF BRANCHING AND EXTINCTION FROM MOLECULAR PHYLOGENIES

Article

Aug 1995
EVOLUTION

Molecular techniques provide ancestral phylogenies of extant taxa with estimated branching times. Here we studied the pattern of ancestral phylogeny of extant taxa produced by branching (or cladogenesis) and extinction of taxa, assuming branching processes with time-dependent rates. (1) If the branching rate b and extinction rate c are constant, the semilog plot of the number of ancestral lineages over time is not a straight line but is curvilinear, with increasing slope toward the end, implying that ancestral phylogeny shows apparent increase in the branching rate near the present. The estimate of b and c based on nonlinear fitting is examined by computer simulation. The estimate of branching rate can be usable for a large phylogeny if b is greater than c, but the estimate of extinction rate c is unreliable because of large bias and variance. (2) Gradual decrease in the slope of the semilog plot of the number of ancestral lineages over time, as was observed in a phylogeny of bird families based on DNA hybridization data, can be explained equally well by either the decreasing branching rate or the increasing extinction rate. Infinitely many pairs of branching and extinction rates as functions of time can produce the same ancestral phylogeny. (3) An explosive branching event in the past would appear as a quick increase in the number of ancestral lineages. In contrast, mass extinction occurring in a brief period, if not accompanied by an increase in branching rate, does not produce any rapid change in the number of ancestral lineages at the time. (4) The condition in which the number of ancestral lineages of extant species changes in parallel with the actual number of species in the past is derived.

Adaptive radiation and molecular systematics: issues and approaches

Article

Jan 1997

Thomas J Givnish

Evolution of species diversity in land communities

Article

Jan 1972

R.H. Whittaker

On the nonprevalence of competitive replacement in the evolution of tetrapods

Article

Jan 1996

Michael J Benton

Phylogenetic systematics of adaptation

Article

Jan 1996
Adaptation

A kinetic model of Phanerozoic taxonomic diversity. I. Analysis of marine orders

Article

Jan 1978
PALEOBIOLOGY

J.J. Jr Sepkoski

A simple equilibrial model for the growth and maintenance of Phanerozoic global marine taxonomie diversity can be constructed from considerations of the behavior of origination and extinction rates with respect to diversity. An initial postulate that total rate of diversification is proportional to number of taxa extant leads to an exponential model for early phases of diversification. This model appears to describe adequately the “explosive” diversification of known metazoan orders across the Precambrian-Cambrian Boundary, suggesting that no special event, other than the initial appearance of Metazoa, is necessary to explain this phenomenon. As numbers of taxa increase, the rate of diversification should become “diversity dependent.” Ecological factors should cause the per taxon rate of origination to decline and the per taxon rate of extinction to increase. If these relationships are modeled as simple linear functions, a logistic description of the behavior of taxonomie diversity through time results. This model appears remarkably consistent with the known pattern of Phanerozoic marine ordinal diversity as a whole. Analysis of observed rates of ordinal origination also indicates these are to a large extent diversity dependent; however, diversity dependence is not immediately evident in rates of ordinal extinction. Possible explanations for this pattern are derived from considerations of the size of higher taxa and from simulations of their diversification. These suggest that both the standing diversity and the pattern of origination of orders may adequately reflect the behavior of species diversity through time; however, correspondence between rates of ordinal and species extinction may deteriorate with progressive loss of information resulting from incomplete sampling of the fossil record.

Adaptive radiation: the interaction of ecological opportunity, adaptation, and speciation

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