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Parent‐Offspring Conflict in the Evolution of Vertebrate Reproductive Mode

June 2004
The American Naturalist 163(5):635-53

June 2004
163(5):635-53

DOI:10.1086/382734

Source
PubMed

Authors:

Bernard J Crespi

Simon Fraser University

We propose and evaluate the hypothesis that parent-offspring conflict over the degree of maternal investment has been one of the main selective factors in the evolution of vertebrate reproductive mode. This hypothesis is supported by data showing that the assumptions of parent-offspring conflict theory are met for relevant taxa; the high number of independent origins of viviparity, matrotrophy (direct maternal-fetal nutrient transfer), and hemochorial placentation (direct fetal access to the maternal bloodstream); the extreme diversity in physiological and morphological aspects of viviparity and placentation, which usually cannot be ascribed adaptive significance in terms of ecological factors; and divergent and convergent patterns in the diversification of placental structure, function, and developmental genetics. This hypothesis is also supported by data demonstrating that embryos and fetuses actively manipulate their interaction with the mother, thereby garnishing increased maternal resources. Our results indicate that selection may favor adaptations of the mother, the fetus, or both in traits related to reproductive mode and that integration of physiological and morphological data with evolutionary ecological data will be required to understand the adaptive significance of interspecific variation in viviparity, matrotrophy, and placentation.

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vol. 163, no. 5 the american naturalist may 2004

Friday Mar 05 2004 01:46 PM/40103/der

Parent-Offspring Conﬂict in the Evolution of

Vertebrate Reproductive Mode

Bernard Crespi

and Christina Semeniuk

†

Behavioural Ecology Research Group, Department of Biological

Sciences, Simon Fraser University, 8888 University Drive, Burnaby,

British Columbia V5A 1S6, Canada

Submitted September 8, 2003; Accepted December 3, 2003;

Electronically published XX

abstract: We propose and evaluate the hypothesis that parent-

offspring conﬂict over the degree of maternal investment has been

one of the main selective factors in the evolution of vertebrate re-

productive mode. This hypothesis is supported by data showing that

the assumptions of parent-offspring conﬂict theory are met for rel-

evant taxa; the high number of independent origins of viviparity,

matrotrophy (direct maternal-fetal nutrient transfer), and hemo-

chorial placentation (direct fetal access to the maternal bloodstream);

the extreme diversity in physiological and morphological aspects of

viviparity and placentation, which usually cannot be ascribed adap-

tive signiﬁcance in terms of ecological factors; and divergent and

convergent patterns in the diversiﬁcation of placental structure, func-

tion, and developmental genetics. This hypothesis is also supported

by data demonstrating that embryos and fetuses actively manipulate

their interaction with the mother, thereby garnishing increased ma-

ternal resources. Our results indicate that selection may favor ad-

aptations of the mother, the fetus, or both in traits related to re-

productive mode and that integration of physiological and

morphological data with evolutionary ecological data will be required

to understand the adaptive signiﬁcance of interspeciﬁc variation in

viviparity, matrotrophy, and placentation.

Keywords: viviparity, parent-offspring conﬂict, placentation, repro-

ductive mode.

Since Aristotle in his Historia Animalium divided animals

into oviparous versus viviparous forms and forms nour-

ished by yolk versus more direct means, analyses of the

ecology, physiology, and evolution of reproductive mode

have remained of considerable interest to biologists (Moss-

* Corresponding author; e-mail: crespi@sfu.ca.

†

E-mail: casemeni@sfu.ca.

Am. Nat. 2004. Vol. 163, pp. 000–000. 䉷 2004 by The University ofChicago.

man 1937, 1987; Wourms 1977, 1981; Wourms et al. 1988;

Blackburn 1992, 1999b, 1999c). Comparative and evolu-

tionary studies have characterized the remarkable diversity

in reproductive mode among animals (Luckett 1976b;

Blu¨m 1986; Blackburn 1999b, 1999c) and have begun to

consider the adaptive signiﬁcance of prenatal mother-off-

spring interactions (Haig 1993, 1996a, 1996b). Ecological

analyses of the evolution of viviparity have traditionally

focused on the costs and beneﬁts of oviparity in compar-

ison with various forms of live birth (e.g., Tinkle and

Gibbons 1977; Shine 1985, 1995) and the role of selection

in optimizing parental investment (e.g., Clutton-Brock

1991). By contrast, physiological and morphological stud-

ies of the evolution of viviparity and placentation have

concentrated on the description, ontogeny, and function

of diverse structures and mechanisms for nutrient transfer

(e.g., Stewart and Blackburn 1988; Wourms et al. 1988;

Wourms and Lombardi 1992; Wourms 1993).

In this article, we integrate comparative, ecological, and

physiological approaches to the evolution of reproductive

mode and propose a new hypothesis that states that parent-

offspring conﬂict (Trivers 1974) has driven the evolution

of vertebrate reproductive mode. Several previous studies

have provided evidence that parental-fetal relationships are

subject to such conﬂict; however, these authors have fo-

cused on the adaptive signiﬁcance of the current forms of

parent-offspring interactions (Trivers 1974; Haig 1993,

1996a, 1996b) or the expected consequences of parent-

offspring conﬂicts for the evolution of polyandry (Zeh and

Zeh 2001) and speciation (Zeh and Zeh 2000; whereby

viviparity-driven conﬂict between mother and fetus pro-

motes antagonistic coevolution, genomic divergence, and

increased postzygotic isolation). Here, we propose that

parent-offspring conﬂict plays a fundamental, causal role

in the evolution of viviparity and placentation and that it

is responsible for much of the diversity in aspects of animal

reproductive mode. We describe the evolutionary dynam-

ics of parent-offspring conﬂict in this context, provide

evidence for our viviparity conﬂict hypothesis, and suggest

further tests using data from physiology, morphology, and

phylogenetics.

PROOF 2 The American Naturalist

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Parent-Offspring Conﬂict over Parental Investment

How is the offspring to compete effectively with its parent?

… Inside the mother the offspring is expected to employ

chemical tactics. (Trivers 1974)

In all organisms where parents and their offspring are not

genetically identical, conﬂicts of interest will arise between

them over the level of parental investment (Trivers 1974).

These phenotypic conﬂicts are mediated by patterns of

gene expression. In mother-offspring interactions, genes

of four sources and kinds may be involved: genes expressed

in the mother, maternally derived genes expressed in the

offspring, paternally derived genes expressed in the off-

spring, and genes expressed in the offspring regardless of

their parental source (Trivers 1974; Haig and Westoby

1989; Haig and Trivers 1995; Haig 1997, 1999b, 2000;

Ubeda and Haig 2003). Each of these types of gene exhibits

its own optimal phenotypic effects for maximizing its rep-

resentation in future generations with regard to how it

inﬂuences the physiological interactions between the

mother and developing embryos.

For the mother, each of her genes has an equal prob-

ability of being present in each offspring, so her best strat-

egy involves allocating nutrients to each offspring over her

lifespan to maximize the aggregate reproductive success of

her descendants. For offspring, the effects of genes are

expected to be more “selﬁsh” such that offspring are se-

lected to seek greater investment from the mother than

she is selected to provide (Trivers 1974; Godfray 1995).

This conﬂict arises because each offspring is more closely

related to itself at (and in the next generation tor p 1

its sons and daughters at ) than it is to any givenr p 0.5

full sibling at (and its nieces and nephews, forr p 0.5

which ). Maternally derived and paternally de-r p 0.25

rived genes in offspring may also exhibit different gene-

expression strategies if such genes are “imprinted” as to

their source (Haig and Westoby 1989; Haig 2000). Thus,

to the extent that a mother’s offspring derive from multiple

paternity within or across broods, genes inherited from a

particular father have a declining probability of being pre-

sent in sibs (Haig 1999b). Such genes should therefore

favor maternal investment in their bearers to an even

greater extent than do maternally derived genes. Evidence

for such imprinting effects on invasive ability of the tro-

phoblast (fetal extraembryonic ectoderm; Mossman 1987,

p. 315) and other aspects of maternal investment has been

described in a variety of taxa (Cross et al. 1994; Bartolomei

and Tilghman 1997; Haig 2000; O’Neill et al. 2000; Vrana

et al. 2001; Tycko and Morison 2002).

Parent-offspring conﬂict is expected to result in off-

spring developing adaptations to extract more from par-

ents than they are selected to provide and adaptations to

compete with siblings over parental resources. The mag-

nitude of such parent-offspring conﬂict can be measured

by the difference between the brood size and degree of

investment per offspring that is optimal for the parent

versus what is optimal for an offspring (Trivers 1974; God-

fray and Parker 1991; Parker 1995). Conﬂict is predicted

to be most intense when only one parent invests, when

the coefﬁcient of relatedness between siblings is low, when

brood size is small, when there is the possibility of intra-

brood competition, and when the beneﬁts of care are non-

depreciable (do not decline with increasing brood size;

Parker 1985, 1995; Godfray and Parker 1991). However,

parent-offspring conﬂict is constrained by the genetic re-

latedness and mutual dependency of the interactants such

that it often involves a tug-of-war over resource allocation,

with signs of conﬂict remaining more or less covert unless

the interactions between parties are perturbed in some way

(Moore and Haig 1991; Haig 1993, 1996a, 1996b).

As in other situations with cooperative interactions en-

tangled with conﬂict and conﬂict constrained by relat-

edness, the evolutionary outcome of parent-offspring in-

teractions is difﬁcult to predict (Parker 1983; Crespi 1992;

Queller 1994; Godfray 1995; Brown et al. 1997; Zeh and

Zeh 2000; Parker et al. 2002b). Such outcomes can depend

on evolutionary starting points, genetic mechanisms, mat-

ing systems, sequences of mutation, the arsenal of traits

in parents and offspring that can be modiﬁed by selection

in this context, and the ﬁtness costs and beneﬁts of win-

ning versus losing in relation to the costs of investing in

adaptations for conﬂict (Haig 1993; Arnqvist and Rowe

2002; Rowe and Arnqvist 2002; Chapman et al. 2003). In

parent-offspring interactions, conﬂicts of interest can be

resolved with one side “winning” (at its optimum) at some

more or less stable intermediate point, or conﬂicts may

generate arms races of variable duration (Parker 1983,

1985; Godfray and Parker 1991; Godfray 1995). Although

parents are usually expected to have an advantage that

derives from size, physical power, and control of resources,

offspring may engage in any number of strategies to ma-

nipulate parents into increased investment; examples in-

clude the release of hormones and other compounds into

the maternal bloodstream (Haig 1993, 1996b) and the loud

begging of nestlings in many species of birds (e.g., Parker

et al. 2002a).

Thus far, most studies of parent-offspring conﬂict have

focused on behavioral interactions, such as soliciting and

siblicide (Trivers 1974; Clutton-Brock 1991; Mock and

Parker 1997). More recently, evidence of physiological

conﬂicts has been described between mothers and pre-

parturition offspring, most notably during human preg-

nancy (Haig 1993). As described by Haig, these maternal-

fetal conﬂicts manifest themselves in the current form of

matrotrophic (direct resource provisioning) viviparity in

Maternal-Fetal Conﬂict PROOF 3

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humans. We argue here that such conﬂicts also reach back

to the origins of maternal investment in vertebrates and

thus should be instrumental in the evolution and diverse

forms of viviparous reproduction itself. By our viviparity

conﬂict hypothesis, the evolution of viviparity has been

driven in part by parent-offspring conﬂict, whereby off-

spring are under continual strong selection to increase the

level of maternal investment that they accrue. Mothers, in

turn, are selected for reproductive modes involving egg

retention and increased investment under appropriate eco-

logical conditions (e.g., Tinkle and Gibbons 1977; Wourms

et al. 1988; Shine 2002) and for increased physiological

efﬁciency in nutrient provision (e.g., Wourms 1993; Tyn-

dale-Briscoe and Renfree 1987), but they are still expected

to favor levels of investment below the optimum for in-

dividual offspring. The main alternative hypothesis to ours

is that the evolution of reproductive modes involving in-

creased investment in individual offspring is driven by

changes in reproductive ecology in the context of how the

physiology and morphology of different lineages can be

modiﬁed by selection. This hypothesis is not mutually ex-

clusive to the viviparity conﬂict idea because ecological

conditions and maternal-fetal interactions are expected to

select sequentially or jointly on reproductive mode. As-

sessing the degree of support for each hypothesis requires

analysis of the mechanisms and selective pressures driving

evolutionary changes in viviparity and placentation.

Vertebrate Reproductive Modes

Living embryos were exceedingly active in utero. They dashed

about, open mouthed, inside the oviduct, snapping at what-

ever they encountered, including the investigator’s hand. In

this case, there was only one embryo in each oviduct. (Wourms

1977)

In oviparous species, preparturition conﬂict is unlikely

because the quantity of yolk and other materials received

by the developing embryo presumably cannot be inﬂu-

enced by genes expressed in the offspring. As a result, the

origin per se of direct maternal investment in developing

embryos and the initial stages of egg retention are pre-

sumably driven by ecological selective pressures. However,

as soon as such investment has evolved, there is potential

for conﬂict if the amount and duration of care received

can be inﬂuenced by genes expressed in the offspring.

Two main nutritional patterns typify the transfer of ma-

ternally derived nutrients in viviparous vertebrates: lecith-

otrophy, in which energy for development is derived from

the yolk of the ovum, and matrotrophy, in which nutrients

are directly supplied by the mother during gestation

(Wourms 1981; Blu¨m 1986; Blackburn 1999b, 1999c).

These nutritional forms are not mutually exclusive, and

the embryos of most viviparous vertebrates are nourished

by some combination of yolk and direct maternal con-

tribution (Wourms et al. 1988; Blackburn 1999c). Matro-

trophic provision of nutrients provides the widest scope

for parent-offspring conﬂict because postzygotic invest-

ment can be substantial, with the developing embryo in

intimate contact with the mother throughout develop-

ment. Matrotrophy can be categorized into three main

forms on the basis of the nutrients supplied to offspring

and how they are delivered (Wourms et al. 1988; Hamlett

1990).

The ﬁrst form, oophagy, whereby the developing fetus

feeds on sibling ova, or adelphophagy, the intrauterine

cannibalism of embryos, is found in some amphibians,

sharks, and teleost ﬁshes (Wourms 1977; Wourms et al.

1988; Blackburn 1992; Gilmore 1993). This reproductive

mode presents opportunities for parent-offspring conﬂict

in that optimal brood sizes may differ between the mother

and offspring (Godfray and Parker 1991, 1992). Because

the offspring are active and in control of cannibalism lev-

els, they may be able to achieve the brood size that max-

imizes their inclusive ﬁtness, and indeed in the sharks and

rays exhibiting oophagy or adelphophagy, only one em-

bryo develops in each of two uterine compartments.

Cannibalistic brood reduction has been described in

other viviparous forms, including some marine snails, cae-

cilians, and other salamanders (Baur 1992; Mock and Par-

ker 1997, pp. 324–333). Although sibling conﬂict typiﬁes

many such cases of this reproductive mode, the degree to

which the interests of mothers and offspring differ remains

unclear because it is difﬁcult in theory and practice to

specify optimal numbers and sizes of offspring for both

parties (Parker et al. 2002b).

The second form, histophagy, involves the ingestion of

maternal secretions by embryos and is characterized by

the absorption of such secretions (Wake 1977; Wourms

1977; Blackburn et al. 1985; Wourms et al. 1988). These

reproductive patterns are found in some sharks and rays,

one anuran, and some caecilians; in addition, monotreme

mammals exhibit an unusual combination of histotrophy

and oviparity because eggs absorb considerable maternal

secretions before deposition (Blackburn 1999c).

Maternal secretions are normally produced from the

uterine epithelium, and the mother is presumably able to

control their constitution and quantity more or less free

of offspring inﬂuence. However, developing offspring may,

in theory, increase the rate of histotroph production in at

least three ways. First, in some amphibians, embryos

abrade the uterine lining with specially adapted prenatal

teeth, apparently to stimulate additional maternal secre-

tions (Wake 1977; Guex and Chen 1986). Like begging

calls in nestlings, such behavior may be partially mala-

daptive for the parents and may lead to investment beyond

PROOF 4 The American Naturalist

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their optimum (Godfray and Parker 1991). Second, ovi-

ductal secretions are under hormonal control in some am-

phibians (e.g., Xavier et al. 1970) such that offspring may

be able to stimulate increased secretion via release of the

same hormones (Haig 1996b). Third, the fetuses of some

rays develop large supranuclear vesicles believed to func-

tion as storage depots for continually ingested secretions

(Hamlett 1999). Such sequestering of maternal resources

may elicit increased investment if it reduces the mother’s

information about offspring’s level of need; indeed, it is

otherwise unclear why a developing ray fetus would store

resources unless they are retained until after parturition.

Similarly, human fetuses sequester unusually high levels

of fat in the last few weeks of pregnancy, after they have

reached full term and are able to survive well postpartur-

ition. (Haig 1993, 1999a). Whether such an apparent ad-

aptation indeed involves conﬂict requires further data.

The third form, placental viviparity, involves transfer of

materials via “any intimate apposition or fusion of the

fetal organs to the maternal (or paternal) tissues for phys-

iological exchange” (Mossman 1937). Placental viviparity

involves nutrient transfer via cell secretions (i.e., histo-

trophic exchange), via blood constituents (hemotrophic

exchange), or by both routes. This reproductive mode is

found in many chondrichthyan and some osteichthyan

ﬁshes, some squamate reptiles, some amphibians (caecil-

ians, frogs, and salamanders), and all therian mammals

(Blu¨m 1986; Blackburn 1999c). The placenta develops

from fetal membranes (the amnion, chorion, allantoic sac,

and yolk sac) and other tissues, and transfer of nutrients

to developing young by this means may be more efﬁcient

physiologically than other methods, although the evidence

for such efﬁciency is meager (Seal et al. 1972; Tyndale-

Briscoe and Renfree 1987, p. 323; Wourms 1993). The

prolonged and intimate contact between mothers and off-

spring engendered by this form of viviparity should pro-

vide offspring with considerable opportunities to inﬂuence

maternal physiology to their own beneﬁt and vice versa

(Zeh and Zeh 2000). The origins and evolution of placental

forms thus provide the clearest context for testing the

assumptions and predictions of the viviparity conﬂict hy-

pothesis, especially because viviparity and placentation ap-

pear to evolve in concert rather than sequentially (Black-

burn 1995, 1998a, 1999c).

Assumptions of the Viviparity Conﬂict Hypothesis

The main assumptions of the viviparity conﬂict hypothesis

are that relatedness between mothers and offspring is less

than unity (the intensity of conﬂict then increases with

multiple paternity within and across broods; Haig 1999b),

that the evolution of viviparity and matrotrophy involve

increased beneﬁts to individual offspring and may also

engender increased costs to mothers, and that offspring

exhibit the ability to manipulate maternal investment in

viviparous and incipiently viviparous forms.

Levels of genetic relatedness between mothers and off-

spring and between offspring are conducive to strong se-

lection for parent-offspring conﬂict over prenatal invest-

ment. Thus, clonal reproduction is rare, and multiple

paternity is virtually the rule among sexual organisms

(Eberhard 1996, p. 413; Birkhead and Parker 1997; Jen-

nions and Petrie 2000; Zeh and Zeh 2001; e.g., in vivip-

arous taxa; Baker et al. 1999; Garner et al. 2002; Saville et

al. 2002). Indeed, multiple paternity may be favored by

one of the same traits that facilitates the evolution of vi-

viparity, internal fertilization (e.g., Wourms et al. 1988).

The possible resultant decrease in paternal investment may

increase the offspring’s optimal level and thus lead to a

higher degree of conﬂict (Parker 1985); multiple paternity

may also generate increased offspring demands through

its effects on the evolution of genomic imprinting (Haig

and Westoby 1989; Haig 1999b, 2000).

Perhaps the most pervasive theme in the literature on

the evolution of viviparity is that it engenders clear beneﬁts

to individual offspring and may impose increased repro-

ductive costs on mothers. Beneﬁts to offspring include

increased survivorship via avoidance of the egg stage, in-

creased size at birth, and increased offspring vigor (e.g.,

Wourms 1977; Shine 1985, 1989, 1995, 2002; Crespi 1989;

Compagno 1990; Guillette 1991; Wourms and Lombardi

1992; Gilmore 1993; Stewart and Thompson 1993; Qualls

and Andrews 1999; Goodwin et al. 2002). These beneﬁts

contrast with numerous costs of reproducing via viviparity,

most of which accrue to mothers; these encompass reduced

foraging ability and higher susceptibility to predation while

pregnant, total brood loss upon death, higher energetic

costs, and lower fecundity (e.g., Wake 1977; Renfree 1983;

Shine 1985, 1989; Compagno 1990; Wourms and Lom-

bardi 1992; Heulin et al. 1994; Blackburn 1995, 2000;

Schwarzkopf 1996; Goodwin et al. 2002; but see also Qualls

and Shine [1998b], who showed that costs of reproduction

apparently did not differ between conspeciﬁc viviparous

and oviparous forms in a lizard). Phenotypic beneﬁts to

mothers of viviparity appear to be relatively few, and they

may include increased energetic efﬁciency in placental

forms (Wourms 1993) and greater ﬂexibility in adjusting

investment level under varying food supplies (Parker 1977;

Low 1978; Renfree 1983; Hayssen et al. 1985; Stewart 1989;

Trexler 1997; Jerez and Ramı´rez-Pinı`lla 2001; but see Rez-

nick et al. 1996). Taken together, these considerations im-

ply that beneﬁts to offspring increase substantially during

the evolution of viviparity and that reproductive costs to

mothers may increase as well.

We suggest that in viviparous and inchoate viviparous

forms, offspring abilities to manipulate the mother are

Maternal-Fetal Conﬂict PROOF 5

Friday Mar 05 2004 01:46 PM/40103/der

even higher before than after birth as a result of the in-

timate, prolonged physiological contact between interac-

tants. Offspring-parent manipulation should ﬁrst become

possible at the point when fetal tissues can release com-

pounds that reach the mother; this may sometimes occur

early in the evolution of viviparity from oviparity, and the

initial effects may be as simple as slightly prolonged egg

retention or embryo-induced changes in osmolarity gra-

dients that contribute to uptake of materials through the

egg capsule (Lombardi et al. 1993; see also Renfree 1977

on concentration gradients across the yolk sac placenta of

a marsupial). Indeed, transfer of materials from mother

to offspring appears common even in the incipient stages

of viviparity (Blackburn 1998b; Stewart and Thompson

2000) such that physiological mechanisms for transfer in

the other direction should not be unexpected on physi-

ological grounds.

The abilities of preparturition human offspring to ma-

nipulate maternal investment are showcased by Haig

(1993, 1999a). As he describes, human fetuses and their

associated tissues secrete myriad factors (e.g., hormones,

steroids, cytokines, and growth factors); these serve, in

humans and other mammals, to signal the presence of the

conceptus, facilitate invasion of the uterine lining, stim-

ulate angiogenesis, locally modulate the mother’s immune

response in the uterus, maintain the early stages of the

pregnancy, and control gestation length (see also Renfree

1977, 1983; Pavia et al. 1979; Hayssen et al. 1985; Clemens

1991; Arcuri et al. 1998, 1999; Lin et al. 2000).

Considerable evidence indicates that abilities of fetuses

to inﬂuence development are not restricted to humans.

Thus, steroid regulation of reproduction by mothers is

present in all vertebrates (Blu¨m 1986; Guillette 1987), and

fetal offspring of elasmobranchs, amphibians, and reptiles

can produce the same or similar compounds as do mam-

mals, apparently with comparable physiological roles in

affecting maternal investment. Guillette (1989) presented

evidence that viviparous nonmammalian vertebrates also

secrete steroids and prostoglandins as pregnancy recog-

nition signals and that embryonic factors inﬂuence ma-

ternal uterine development in various ways apparently

beneﬁcial to the fetus. Hamlett (1999) noted that the pla-

centa of some sharks secretes steroid hormones and that

the yolk sac placenta (the simplest form of placentation)

exhibits tissues that also appear to produce steroids, and

Callard and Koob (1993), Callard et al. (1993), and Koob

and Callard (1999) provided additional evidence for ster-

oid regulation of elasmobranch reproduction, with poten-

tial effects from the fetus. Even under the seemingly sim-

plest form of viviparity, histophagy, as expressed in a

species of salamander, antagonistic maternal immune re-

actions (rejection and facilitation) toward the embryo have

been found, along with immunosuppressive factors in the

pregnancy serum thought to originate from the embryo

(Chateaureynaud et al. 1979; Badet 1984). A range of cy-

tokines and other hormones, which regulate immune re-

sponses, fetal growth, and differentiation in mammals, has

also been identiﬁed at the maternal-fetal interface in a

species of placental reptile (Paulesu et al. 1995; Paulesu

1997; Jones et al. 2003). Painter and Moore (1999) re-

ported the production of progesterone and corticosterone

from the reptilian fetal adrenal gland and suggested that

the fetal placenta metabolizes steroid hormones, and Bon-

net et al. (2001) reported that progesterone plays an im-

portant role in the pregnancy of a viviparous snake by

stimulating vascularization of the oviducts. Endocrinol-

ogical studies of a placental skink and a review of other

reptiles (Guarino et al. 1998) have shown that when the

corpus luteum begins to degenerate after the middle of

pregnancy, the placenta can become an endocrine organ,

and, as in some mammals, it begins to replace and main-

tain the high levels of progesterone circulating in maternal

blood. Moreover, young embryos of the reptile Lacerta

vivipara produce a compound that extends the life of the

corpus luteum (and thus gestation length; Xavier et al.

1988), and embryos of other lizards release a variety of

compounds, often early in development (see Guillette

1992). Callard et al. (1992) noted that oviparous groups

(e.g., skates, turtles, and birds) exhibit a predominantly

preovulatory pattern of progesterone production, whereas

those groups in which viviparity has evolved (e.g., sharks,

snakes, and lizards) exhibit mainly a postovulatory pattern.

Finally, Shine and Guillette (1988) present evidence that

in reptiles, increased duration of progesterone secretion

prolongs egg retention, which may serve as a simple mech-

anism for the initial stages in the evolution of viviparity.

Their model is of special importance for the viviparity

conﬂict hypothesis, given that progesterone can also be

secreted by reptile fetuses. Offspring of oviparous and vi-

viparous reptiles may also beneﬁt from delaying birth,

potentially beyond the maternal optimum in viviparous

forms, and they may thus control this important aspect

of development (Shine and Olsson 2003).

These cases indicate that preparturition offspring of all

major vertebrate groups exhibiting viviparity demonstrate

abilities to or the potential to manipulate maternal repro-

ductive physiology. Thus, the assumptions of the viviparity

conﬂict hypothesis appear to be satisﬁed. The hypothesis

makes three main predictions that can be evaluated with

the available data: multiple origins of viviparity and forms

of placentation, extreme diversity in traits related to fetal-

maternal interactions among vivparous forms, and evi-

dence of fetal-maternal conﬂict over levels of investment,

which may lead to arms races.

PROOF 6 The American Naturalist

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Multiple Origins of Viviparity and

Forms of Placentation

Once egg retention exists, maternal oviductal and ovarian

function could be modiﬁed by responding to embryonic fac-

tors. (Guillette 1989)

One of the hallmarks of strong selection is parallel or

convergent evolution (Schluter and Nagel 1995; Losos et

al. 1998; Madsen et al. 2001; Nosil et al. 2002). This evo-

lutionary pattern implies ﬁrst that selection, rather than

the chance effects of drift, has given rise to a particular

trait and second that diverse lineages have been similarly

transformed, overcoming lineage-speciﬁc constraints on

many occasions. Multiple origins of viviparity, matrotro-

phy, and more invasive placentation may be explicable by

both the viviparity conﬂict and reproductive ecology hy-

potheses, and they provide indirect support for viviparity

conﬂict to the degree that they cannot be explained by

variation in ecological conditions. In addition, more or

less unidirectional trends from oviparity to viviparity and

to increased investment in viviparous forms suggest either

that such transitions are irreversible due to their genetic

or physiological architecture (Bull and Charnov 1985; Lee

and Shine 1998) or that strong selection on offspring can

prevent them.

Striking parallelism and convergence are found in the

origins of viviparity itself, the origins of placentation, and

the forms of placentation most conducive to offspring

control over parental investment. Among vertebrates, vi-

viparity has evolved more than 120 times; there are more

than 100 inferred transitions in reptiles, 12 in teleost ﬁshes

(including patrotrophic viviparity in some seahorses;

Blackburn 1999c; Wilson et al. 2003), nine to 10 in sharks

and rays, ﬁve in amphibians, and apparently two in mam-

mals (Hayssen et al. 1985; Dulvy and Reynolds 1997; Zeller

1997, 1999; Blackburn 1999b, 1999c; Goodwin et al. 2002;

Reynolds et al. 2002). Matrotrophy has also evolved readily

(23–24 times), with at least three inferred origins in rep-

tiles, 12 in teleost ﬁshes, four to ﬁve in sharks and rays,

three in amphibians, and one in mammals (Dulvy and

Reynolds 1997). In some lineages, viviparity is character-

istic of higher taxonomic categories (e.g., eutherian and

metatherian mammals and some elasmobranch groups);

however, in other taxa, it varies among closely related spe-

cies or even among populations (e.g., Blackburn 1992,

1993, 1995, 1998a; Heap 1994; Qualls et al. 1995; Surget-

Groba et al. 2001). The transitions between oviparity and

viviparity appear to be virtually unidirectional because

there is evidence of shifts from viviparity back to oviparity

in only a few cases, and even these are ambiguous (de

Fraipont et al. 1996, 1999; Dulvy and Reynolds 1997; Lee

and Shine 1998; Blackburn 1999a; Surget-Groba et al.

2001; Reynolds et al. 2002; Douady et al. 2003).

Viviparity has been linked more or less closely to en-

vironmental factors in several taxonomic groups. Thus, in

reptiles, viviparous forms are most common in relatively

cold climates (Tinkle and Gibbons 1977; Shine and Bull

1978; Shine 1985, 2002 and references therein), and in

elasmobranchs, viviparity and matrotrophy are found

most often in tropical and subtropical waters (Wourms

1977; Clutton-Brock 1991; Dulvy and Reynolds 1997),

where utilization of yolk by embryos may be energetically

inefﬁcient (Dulvy 1998). By contrast, reproductive mode

is apparently not associated with ecomorphotype in sharks

(Compagno 1990), and Wourms et al. (1988) noted that

for teleost ﬁshes, “it is difﬁcult to correlate viviparity …

with speciﬁc ecological parameters.” Indeed, Shine and

Berry (1978), Shine (1985, 1987), and Packard et al. (1989)

stressed that the current ecology of viviparous forms pro-

vides only indirect evidence for the role of speciﬁc envi-

ronmental factors in the origins of this reproductive mode.

Thus, although viviparity itself is clearly adaptive in harsh

environments for eggs among some taxa, the selective ad-

vantages of transitional stages in the origin of viviparity

are often unclear (Shine and Bull 1979; Shine 1985; Smith

and Shine 1997; see also Blackburn 1982), and the eco-

logical adaptive signiﬁcance of the different forms of vi-

viparity or matrotrophy has been difﬁcult to elucidate

(Wourms et al. 1988; Guillette 1991; Stewart and Thomp-

son 2000).

Blackburn (1995, 1998a) provides evidence that inter-

mediate transitional stages in the evolution of viviparity

and placentation are rarely found among extant forms

such that they appear to evolve rapidly. His hypothesis is

also supported by the ﬁnding of Reynolds et al. (2002),

who used phylogenies to infer that evolutionary changes

in elasmobranch viviparity often proceeded directly from

egg laying to matrotrophic viviparity and the emphasis by

Rothchild (2003) on the great gap between metatherian

and eutherian reproductive modes. Moreover, Mossman

(1987, p. 146) points out that little morphological change

in fetal membranes is required for the transition to vivi-

parity because most of the changes are mediated by phys-

iological shifts. By the viviparity conﬂict hypothesis, eco-

logical factors need not drive transitions to viviparity and

matrotrophy in isolation because an advantage will always

be present for offspring to accrue additional investment

up to their optimal level. Moreover, selection on offspring

and mothers is apparently strong enough to cause rapid

microevolutionary change, which has led to accelerated

among-population divergence and speciation in some taxa

such as mammals (Zeh and Zeh 2000).

Placentation has evolved concomitantly with viviparity

among vertebrates (Blackburn 1995, 1999b, 1999c), and it

Maternal-Fetal Conﬂict PROOF 7

Friday Mar 05 2004 01:46 PM/40103/der

exhibits the same pattern of multiple evolutionary origins,

with many striking cases of convergence and parallelism

(e.g., Wourms 1977; Blackburn et al. 1984; Wourms et al.

1988; Wourms and Lombardi 1992; Blackburn 1993,

1999b, 1999c; Meyer and Lydeard 1993; Reznick et al. 2002;

also Wourms and Cohen 1975 on trophotaeniae, a pla-

cental analogue in some ﬁshes). There are three main

forms of placentation with regard to one of its most fun-

damental aspects, the functional morphology of the ma-

ternal-fetal interface: epitheliochorial placentation, which

involves proliferation of the trophoblast and uterine epi-

thelium with little or no invasiveness of the trophoblast

into maternal tissue; endotheliochorial placentation,

whereby the trophoblast invades maternal tissue but does

not penetrate into the bloodstream; and hemochorial plac-

entation, in which the trophoblast invades far enough for

the developing placenta to gain direct access to maternal

blood (e.g., Luckett 1976b; Mossman 1987; King 1992).

Hemochorial placentation entails the greatest opportuni-

ties for offspring to manipulate the mother toward in-

creased investment; offspring have direct access to mater-

nal nutrients in the blood, they may release compounds

into her bloodstream, and they can distinguish between

maternal versus fetal sources of hormones and other sub-

stances, while mothers may remain ignorant of this im-

portant information (Haig 1991, 1993, 1999a; Kurz et al.

1999).

Hemochorial placentation has apparently originated at

least eight times in mammals, among ﬂying lemurs, bats,

rodents and lagomorphs, primates, anteaters and arma-

dillos, hyraxes, tenrecs and elephant shrews, and hedge-

hogs (King 1992; Carter 2001); only in some rodents has

hemochorial placentation apparently been lost, given rise

to an endotheliochorial form (Mess 2003). Similarly, a

species of shark has evolved a unique form of hemochorial

placenta (Wourms 1993), the placentae of some reptiles

may approach (though not reach) the hemochorial state

(Luckett 1976b; Mossman 1987 p. 146; Blackburn 1993),

and some metatherians (e.g., bandicoots and fat-tailed

dunnarts) exhibit an invasive placenta that has evolved

convergently with that of eutherians (Luckett 1976b; Ren-

free 1983; Hayssen et al. 1985; Tyndale-Briscoe and Renfree

1987; Roberts and Breed 1994a, 1994b; Zeller 1999). Black-

burn et al. (1985) comment on the “convergent trends

toward reduction of the distance between fetal and ma-

ternal bloodstreams in numerous placental groups” (see

also Wourms and Lombardi 1992), which ultimately re-

sults in hemochorial forms. Finally, Pijnenborg et al.

(1981) describe the convergent evolution, in rodents and

humans, of invasion into the maternal spiral arteries of

trophoblast cells, which modify the arteries such that blood

ﬂow cannot be restricted (see also Haig 1993).

Carter (2001) remarks that in hemochorial forms, the

“prime function of the trophoblast is to adapt maternal

circulation to the needs of the placenta and growing fetus.”

They stated that “the advantage of reducing the number

of layers in the interheme membrane is clearly great

enough for such adaptations to have been selected many

times.” But if such an advantage exists, presumably it

should be more common among mammals rather than

distributed so sporadically. By contrast, Mossman (1987,

pp. 152–153, 296) notes that there is no clear selective

advantage associated with variation in trophoblast inva-

siveness, and Pijnenborg et al. (1985) state that it is difﬁcult

to attach any adaptive advantage to the differences among

the three forms of placentation. Leiser and Kaufmann

(1994) describe how neonatal/placental weight ratios are

uncorrelated with the number of tissue layers separating

maternal and fetal blood but are apparently associated with

the geometry of maternal-fetal blood ﬂow interrelation-

ships; moreover, high daily fetal growth rates per placental

weight appear to require a relatively efﬁcient placenta

(hemochorial or endotheliochorial). These ﬁndings sug-

gest that placental form inﬂuences aspects of fetal devel-

opment related to maternal input, although the ecological

disparities among the mammals with hemochorial plac-

entation argue against the presence of ecological correlates.

According to the viviparity conﬂict hypothesis, there

may indeed be no ecologically based selective difference

among the three placental forms. Thus, such differences

arise because only in some lineages have fetuses been able

to gain access to the maternal bloodstream; the current

outcomes of conﬂict vary among taxa, depending on dif-

ferences in physiological and morphological starting

points, sequences of mutational events, strengths of selec-

tion on the interacting parties, and the presence and form

of other adaptations. Consistent with this hypothesis, hem-

ochorial placentation is reached by quite different devel-

opmental pathways across these mammal groups (Carter

2001).

Rampant Diversiﬁcation of Viviparity and Placentation

There is no other mammalian organ whose structure and func-

tion are so species diverse as those of the placenta. This is

curious since the “purpose” of the placenta, presumably, is

the same in all species. (Faber et al. 1992)

The viviparity conﬂict hypothesis implies antagonistic co-

evolution between parents and offspring in traits that in-

ﬂuence prenatal investment. Thus, after microevolution

toward viviparity and matrotrophy has begun, these traits

are expected to evolve rapidly and in a manner that may

be difﬁcult to predict from comparative or ecological data,

exhibiting similar evolutionary dynamics to those en-

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PROOF 8 The American Naturalist

Friday Mar 05 2004 01:46 PM/40103/der

countered in other cases of antagonistic coevolution, such

as sexual conﬂict (Brown et al. 1997; Arnqvist and Rowe

2002; Rowe and Arnqvist 2002; Chapman et al. 2003) or

host-parasite interaction (Hughes 1991; Haraguchi and Sa-

saki 1996; Buckling and Rainey 2002). Although parent-

offspring strife is constrained by genetic relatedness, it

should nonetheless generate high diversity in morpholog-

ical, physiological, developmental, and genetic aspects of

reproductive mode.

Forms of viviparity itself exhibit notable diversity within

eutherian mammals (Rothchild 2003), squamate reptiles

(Blackburn 1993), caecilians (Laurin et al. 2000), other

amphibians (Wake 1977; Wake and Dickie 1998), and

ﬁshes (Wourms 1977, 1981; Wourms et al. 1988; Com-

pagno 1990; Wourms and Lombardi 1992; Hamlett and

Hysell 1998; Hamlett 1999). Such diversity extends across

all taxonomic levels because closely related species, pop-

ulations, or individuals within populations often differ

substantially in fundamental aspects of reproductive mode

(e.g., Guillette 1981; Packard et al. 1989; Blackburn 1992,

1993, 1995, 1998a; Heap 1994; Pinella and Laurent 1996;

Meisner and Burns 1997; Smith and Shine 1997; Trexler

1997; Fairbairn et al. 1998; Stewart and Thompson 2000;

Swain and Jones 2000; Thompson et al. 2000; Smith et al.

2001; Reznick et al. 2002).

Although the basic hormones involved in regulation of

reproductive processes are highly conserved among ver-

tebrates, the sources, functions, and targets of these hor-

mones differ strikingly among taxa, sometimes between

closely related species. Thus, Blu¨m (1986), Callard et al.

(1992), Cross et al. (1994), and Roberts et al. (1999) de-

scribe the wide range of hormonal mechanisms vertebrate

embryos use to help maintain pregnancy. Rothchild (1981)

noted how among species of mammals, the regulation of

preovulatory follicles has remained conservative, while the

regulatory mechanisms for postovulatry follicles (after ma-

ternal-fetal conﬂict has begun; Haig 1993) differ widely.

Guillette (1989) describes some of the profound differ-

ences among humans, pigs, and sheep in the chemical

signals used for recognition of pregnancy (see also Freyer

et al. 2003), and Heap (1994) describes how mammal

species are remarkably dissimilar in the mechanisms

whereby immunological rejection of the conceptus is

achieved. Haig (1993) and Stewart and Allen (1995) de-

scribe the convergent evolution of chorionic gonadotro-

pins in primates and horses, and Forsyth (1994) describes

the convergent evolution of placental lactogens, which are

involved in diversion of nutrients to the fetus, in primates,

rodents, and ruminants. Finally, Amoroso (1981), Heap

(1994), Meyer (1994), and Blackburn (2000) describe no-

table variation in the sources, levels, and proﬁles of pro-

gesterone during gestation; for example, progesterone ap-

pears to regulate reproduction differently even among

closely related snakes in garter snakes (Highﬁll and Mead

1975; Whittier et al. 1987; also see Bonnet et al. 2001).

These patterns imply strong divergent and convergent se-

lection on the production levels, targets, and functions of

reproductive hormones involved in maternal-fetal inter-

action (see also Haig 1996b), which appears difﬁcult to

attribute to ecological causes even though an absence of

evidence cannot be interpreted unambiguously as the

converse.

Trophoblasts of therian mammals differ profoundly

even among closely related species in the chemical signals

that they produce (Packard et al. 1989; Heap 1994); in

their expression sites for growth factors (Carter and Han

1999); in the presence, density, and form of their “giant

cells” (Mossman 1987, p. 298); and in their degree of

invasiveness into the uterine lining (Hughes 1974; Luckett

1976b; Pijnenborg et al. 1981, 1985; Heap 1994; Carter

2001; Allen et al. 2003; Freyer et al. 2003). Moreover, in

accordance with different resolutions of conﬂict over in-

vestment or ongoing conﬂict, the degree of invasiveness

is determined in diverse ways among taxa “by properties

of the trophoblast itself, by maternal factors such as de-

cidualization, by pregnancy-induced change of other uter-

ine tissues, and by maternal immune responses” (Pijnen-

borg et al. 1981).

The placenta exhibits greater interspeciﬁc variation in

morphology than does any other mammalian organ (e.g.,

Benirschke 1983; Mossman 1987; Faber et al. 1992; Leiser

and Kaufmann 1994). This remarkable variation among

species in the development, physiology, and morphology

of placentae has fascinated and puzzled biologists for more

than 50 yr (Mossman 1937, 1987, p. 150; Luckett 1976b;

Renfree 1977; Pijnenborg et al. 1985; Stewart and Black-

burn 1988; Wourms et al. 1988; King 1992; Allen et al.

2003). The main source of such puzzlement is that the

physiological and morphological vicissitude of placenta-

based interactions is accompanied by simplicity of primary

function: transfer of nutrients (Faber et al. 1992). Much

of the variation in placental morphology is due to diversity

in the deﬁnitive forms of homologous or analogous struc-

tures, but much is also generated via heterochronic shifts

and the terminal addition of new stages (Luckett 1976b;

Wourms et al. 1988; Wourms 1993; Stewart and Thompson

1996, 2003; Allen et al. 2003), which provides an additional

dimension for diversiﬁcation. Here, we propose that the

striking interspeciﬁc diversity of placental physiology and

morphology reﬂects a long evolutionary history of ma-

ternal-fetal conﬂict. Evaluating this hypothesis requires

consideration of the mechanisms of interaction at the ma-

ternal-fetal interface.

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Maternal-Fetal Antagonism at the Placental Interface

One reason why the placenta and placental signalling mole-

cules … are evolving so quickly may be because the placenta

is the site of considerable genetic experimentation. If the re-

lationship between the mother and the conceptus possesses

elements of conﬂict, rather than being strictly nourishing, a

change in one side of the placenta will in all likelihood be

accompanied by a counter-move on the other side. (Roberts

et al. 1999)

Roberts et al. (1999) anticipate the viviparity conﬂict hy-

pothesis and one of the best means to test it: ﬁnding more

or less direct evidence of maternal-fetal antagonism man-

ifested in the genetics, physiology, and morphology of the

placenta, the uterus (or analogous structure), and the hor-

mones and other chemical factors that mediate their in-

teractions. The conﬂict hypothesis makes several predic-

tions regarding this fetal-maternal interface: the presence

of placental and maternal structures and functions that

reﬂect a tug-of-war of constrained reciprocal antagonism

(Haig 1993, 1996a, 1996b, 1999a), a positive association

between placental complexity and maternal investment,

higher interspeciﬁc variation in the placental traits that are

most closely related to resource transfer, and rapid evo-

lution and positive selection on placentally expressed genes

and maternally expressed genes that interact with the fetus.

Reciprocal maternal-fetal antagonism is manifested in

the ﬁrst stage leading to placentation, association of the

trophoblast with the uterine lining. In mammals, increased

fetal (trophoblast) invasiveness has apparently been coun-

tered over evolutionary time by three responses: maternal

secretion of compounds to reduce its degree (Heap 1994),

which includes a stronger maternal immune response (Pi-

jnenborg et al. 1981; Leiser and Kaufmann 1994; Stewart

and Allen 1995); the evolution of more developed maternal

epithelial barriers (Pijnenborg et al. 1995); or the shedding

of overly invasive trophoblasts with the uterine lining (Pi-

jnenborg et al. 1981; Haig 1993, 1996a; Finn 1998). More-

over, as described by Pijnenborg et al. (1985), pigs exhibit

noninvasive trophoblasts, but if a trophoblast is trans-

planted to an ectopic site, it invades maternal tissue, ex-

pressing cytolytic and phagocytic properties that are ap-

parently suppressed by the mother in normal pregnancies

(Pijnenborg et al. 1981). Similarly, a mouse trophoblast

(which is normally mildly invasive) invades uncontrollably

when transplanted to ectopic sites (see Cross et al. 1994).

These ﬁndings suggest that invasiveness reﬂects a tug-of-

war between mother and fetus, with adaptations on both

sides to restrain the other; this hypothesis can be evaluated

more directly by analyzing trophoblast invasiveness and

maternal responses in a species-level phylogenetic context.

Among eutherian and metatherian mammals studied to

date, the trophoblast and developing placenta begin to

secrete hormones early in ontogeny. Some of these hor-

mones function as signals for maternal recognition of

pregnancy (e.g., Heap et al. 1981; Guillette 1989; Allen and

Stewart 2001), which may represent simple fetally derived

hormonal signals to the mother that a fetus is present,

serving to maintain the pregnancy but also perhaps func-

tioning as a test of embryo quality imposed by mothers

(i.e., ability to produce large amounts of gene product

quickly; Haig 1999a). In either case, the developing con-

ceptus should be under strong selection to manipulate the

mother, given any degree of conﬂict over whether a par-

ticular incipient pregnancy will proceed and how much

will be invested in the fetus. Such conﬂict apparently un-

derlies the evolution and function of equine chorionic

gonadotropin, which is produced in large quantities by a

placental structure (the endometrial cups) unique to

horses (Haig 1993; Stewart and Allen 1995). This hor-

mone, which appears to be produced by a paternally im-

printed gene (Allen et al. 1993; Lennard et al. 1995), ex-

hibits low binding afﬁnity to its maternal receptors, and

analysis of experimental hybrid pregnancies between

horses and donkeys provides evidence that the maternal

receptors of horses have evolved to become recalcitrant to

this fetal hormone to prevent overstimulation of the ova-

ries (Haig 1993; Stewart and Allen 1995). Moreover, anal-

yses of hybrid and normal pregnancies show that equine

chorionic gonadotropin is not essential for the completion

of development, though its absence is associated with in-

adequate placentation and high levels of abortion (Stewart

and Allen 1995; Allen 2001; Allen and Stewart 2001); the

analyses also show that the development of the endome-

trial cups depends in part on the genotype of the uterus

(Allen et al. 1993; Allen and Stewart 2001), suggesting that

the mother has evolved some degree of control over their

growth and that the mother’s immune system destroys the

endometrial cups about a month after they are formed

(Allen 2001). During the second half of gestation, the horse

fetus also undergoes a massive, temporary enlargement of

the gonads, which produce large quantities of oestrogens;

as with equine chorionic gonadotropin, production of this

hormone by the fetus is not essential for development.

However, fetuses with their gonads removed developed

into smaller foals, apparently as a result of reduced uter-

oplacental blood ﬂow (Allen 2001; Allen and Stewart

2001).

Haig (1993, 1996b) presents evidence from human preg-

nancy that antagonistic coevolution may explain the re-

markably high levels of some products secreted by the

placenta, the secretion by the placenta of some of the same

hormones that mothers are also producing (thereby mask-

ing the source of the secretions), and the production of

gene products that are rapidly inactivated by the mother.

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PROOF 10 The American Naturalist

Friday Mar 05 2004 01:46 PM/40103/der

Moreover, Painter et al. (2002) found that the placenta

buffers the effects of experimental variation in maternal

steroid concentration in a viviparous reptile and that ma-

ternal hormones may inhibit placental hormone secretion.

These results hint at the presence of antagonistic inter-

actions whereby each party can undermine the endocrine

production strategies of the other. This evidence from

horses, humans, and a reptile suggests that the evolution

of endocrine hormone production has involved consid-

erable conﬂict between mothers and fetuses, which can be

resolved in diverse ways.

By our hypothesis, the striking interspeciﬁc variation in

placental morphology (reviewed for mammals in Moss-

man 1987) also reﬂects the outcomes of maternal-fetal

conﬂict over investment (see also Kurz et al. 1999; Zechner

et al. 2004). Presently, our clearest prediction is that the

placental traits that vary most among taxa will be those

most closely associated with control over nutrient transfer

because on these traits antagonistic selection has been

strongest. The many origins among mammals of hemo-

chorial placentation concord with this prediction, as does

the presence of unique structures such as the equine en-

dometrial cups. Moreover, among placental skinks, there

is a positive association between placental complexity

(which may reﬂect adaptations for conﬂict) and the extent

of nutrient transfer (Thompson et al. 2000, 2002). How-

ever, this prediction is difﬁcult to test because the func-

tional morphology of placentation has been analyzed in

sufﬁcient detail to ascribe adaptive signiﬁcance to taxon-

speciﬁc placental structures in only a few taxa: humans

(Haig 1993, 1999a), mice (Rossant and Cross 2001), horses

(Allen 2001; Allen and Stewart 2001), and some other farm

animals (Allen et al. 2003). Indeed, the byzantine com-

plexity and puzzling details of placental development in

humans and horses, two of the best-studied species, sug-

gest that robust comparative analyses of the adaptive sig-

niﬁcance of variation in placental phenotypes must await

further study directed toward clades such as primates, ro-

dents, and artiodactyls, where much of the descriptive

groundwork has already been laid.

Maternal-fetal conﬂict may also be expressed in the de-

velopment of new fetal structures, some of which are anal-

ogous to the placenta. Thus, the appendiculae of some

placental sharks, outgrowths of the umbilical cord that

appear to function as an additional, secondary placenta

(Wourms et al. 1988; Hamlett 1989, 1990, 1999; Wourms

and Lombardi 1992; Lombardi et al. 1993; Wourms 1993),

may also represent an effect of maternal-fetal coevolution

if they originated in response to maternal limitations im-

posed on the original placental interface (Southwell and

Prasad 1919). Appendiculae appear to have a secretory

role in some species (Hamlett 1989, 1990, 1999), which

the viviparity conﬂict hypothesis predicts will involve ma-

nipulation of the mother to increase nutrient provision

(e.g., Haig 1996b). They also exhibit striking morpholog-

ical diversity among species, and in at least one shark

genus, they are present in some species but not others

(Hamlett 1989). Some placental structures of therian

mammals that may be comparable to appendiculae in ap-

parently facilitating absorption of nutrients include “in-

verted yolk sacs, hematomes, areolae, arcade networks, and

marginal folds of chorioallantois around the placentomes”

(Mossman 1987, p. 297); these structures also vary notably

among mammalian groups in their presence and forms

(see also Allen 2001 on multiple sources of nutrient trans-

fer in horses). By our hypothesis, some or all of these

structures evolved in the context of offspring under strong

selection to develop new routes for increased maternal

investment. Similarly, the functional redundancy of diverse

biochemical factors involved in mammalian implantation

(Vigano` et al. 2003) may reﬂect recruitment of new mech-

anisms for trophoblasts to successfully invade the uterine

lining.

At the molecular level, numerous genes involved in

mammalian maternal-fetal interactions evolve especially

rapidly (Haig 1993; Chun et al. 1999; Roberts et al. 1999;

Wallis 2000; Sol-Church et al. 2002; see also Kurz et al.

1999). However, imprinted genes analyzed thus far show

no evidence of antagonistic coevolution (McVean and

Hurst 1997; but see Paldi 2003; Verona et al. 2003), perhaps

because they fulﬁll essential functions in contexts other

than fetal development (Rossant and Cross 2001; Cross et

al. 2003). Antagonistic coevolution may also be responsible

for the strong positive selection detected in the evolution

of numerous placentally expressed genes (Ohta 1993; Wal-

lis 1993; Hurst 1994; Maiti et al. 1996; Xie et al. 1997;

Garbayo et al. 2000; Hughes et al. 2000; Maston and Ru-

vulo 2002; Zhang and Rosenberg 2002; Zhang et al. 2002),

dramatic escalations in rate of change of maternal hor-

mones associated with the origins of placental hormones

(Wallis 1981, 1993, 1994, 1996, 1997, 2000; Lioupis et al.

1997; Wallis et al. 2001), and the co-option of endogenous

retroviruses for regulating the placental expression of genes

involved in immunosuppression and trophoblast inva-

siveness (Harris 1998; Bie`che et al. 2003). Joint analysis

of such molecular evolutionary changes with the evolution

of placental and maternal endocrine regulation and pla-

cental morphology may be especially useful for under-

standing how placental traits originate and evolve. Such

analyses should also yield implications for human health

and reproduction because miscarriages are frequently

caused by disruptions of placental development (e.g., Ros-

sant and Cross 2001), because trophoblast invasion of the

uterine wall provides useful models for understanding im-

munology and carcinogenesis (e.g., Ohlsson 1989; Barnea

and Brusato 2000), because parent-offspring and intra-

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Maternal-Fetal Conﬂict PROOF 11

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genomic conﬂict apparently favor the evolution of alleles

that promote cancer (Summers et al. 2002), and because

adult health increasingly appears to be programmed by

the environment and epigenetics of fetal development

(e.g., Godfrey 2002).

Considered together, the evidence from studies of im-

plantation, hormone production, placental structure, evo-

lution of accessory structures for matrotrophic exchange,

and molecular evolution suggest that maternal-fetal arms

races may be widespread, at least in elasmobranchs and

placental vertebrates. Analysis of how and why these are

resolved or continue unabated remains a challenge for

future work.

Alternative Hypotheses

Tentatively, the most reasonable general hypothesis (for the

evolution of placental diversity) seems to me to be that the

genotypes of each group differently limit the directions evo-

lution can take. (Mossman 1987, p. 293)

The diverse forms of viviparity and placentation may also

represent multiple adaptive peaks structured by ecological

selective pressures in the context of different morpholog-

ical and physiological starting points. Testing this hypoth-

esis requires drawing comparative connections between

aspects of ecology and the physiological details of repro-

ductive mode. Similarly, the role of disparate physiological

and morphological evolutionary starting points for the

evolution of viviparity among the major vertebrate groups

in generating diversity requires further study. The amniote

egg is, however, fundamentally similar among vertebrates

(e.g, Luckett 1976b; Mossman 1987), and the profound

differences in reproductive physiology between closely re-

lated or conspeciﬁc forms argue strongly against the pri-

macy of diverse starting points in producing adaptively

similar but diverse extant forms. Indeed, the problem of

matrotrophic viviparity appears to be considerably more

complex than efﬁcient nutrient transfer to developing off-

spring; to the extent that the viviparity conﬂict hypothesis

holds true, the reproductive strategies of mothers and off-

spring are mutually problematic because physiological ef-

ﬁciency serves as both a constraint on conﬂict and a se-

lective pressure itself.

Further evaluation of the viviparity conﬂict hypothesis,

in relation to alternatives, may best proceed along several

fronts. First, Haigian analyses of physiological mechanisms

of maternal-fetal interaction and genomic imprinting ef-

fects in nonhuman mammals and other viviparous ver-

tebrates (Haig 1993; Haig and Trivers 1995) would dem-

onstrate the generality of conﬂict. Such studies would be

especially useful in species that are presumed or inferred

to be plesiotypic for their forms of viviparity or placen-

tation because they would show the potential role of con-

ﬂict in the early stages of transition between reproductive

modes. Second, the fetal-maternal arms race hypothesis

requires phylogenetically based tests, which would most

directly demonstrate effects of antagonistic coevolution. A

phylogenetic perspective on the evolution of the placenta

is already available (Luckett 1976a, 1976b, 1993; Mossman

1987; Carter 2001; see also Thompson et al. 2002; Mess

et al. 2003) and may serve as a template for such analyses.

However, the high diversity of placental traits urges cau-

tion in the use of such traits to infer phylogenies them-

selves (e.g., Luckett 1976a; Mossman 1987) and in the use

of animal models for understanding human placentation

(e.g., Faber et al. 1992; Rossant and Cross 2001). Third,

given that conﬂict over reproductive mode may affect evo-

lutionary trajectories, it may have important macroevo-

lutionary consequences. For example, might metatherians

have evolved in the context of mothers winning in most

aspects of conﬂict over control of investment via short

gestation and long lactation (Hayssen et al. 1985; Renfree

1977, 1983)? Did the allantois itself originate in viviparous

forms as a result of the evolution of this reproductive mode

(Mossman 1987, pp. 118, 124–126)? Given that fetal mem-

branes and placental structure are relatively uniform

within mammalian families but extremely different among

them (Mossman 1987, p. 122, 288–290), might they be

involved in the origin of higher mammalian taxa? Fourth,

Zeh and Zeh (2000) provide evidence that viviparity-in-

duced conﬂicts have led to accelerated speciation in mam-

mals via rapid divergence of traits involved in maternal-

fetal interactions (see also Wilda et al. 2000); are viviparous

clades of vertebrates more or less speciose than their ovip-

arous sister taxa (Slowinski and Guyer 1994)? Finally, tests

for ecological differences between closely related species

or populations that differ in aspects of viviparity, matro-

trophy, and placentation may reveal unforseen adaptive

linkages or evidence that the differences reﬂect divergent

outcomes of conﬂict. Given that antagonistic coevolution

is expected in the evolution of traits related to viviparity

and matrotrophy, analyses of their adaptive signiﬁcance

may often be misled by genetic conﬂict in the guise of

ecological maladaptation. Moreover, changes in repro-

ductive mode as a result of maternal-fetal conﬂict may

also affect the ecology of a species (J. Reynolds, personal

communication) such that differentiating causes from ef-

fects becomes difﬁcult.

Our main goal has been to provide a new perspective

on the diversiﬁcation of vertebrate reproductive modes.

Most generally, we have shown that analysis of reproduc-

tive mode provides a novel opportunity for analysis of

how conﬂicts are resolved or ongoing between parties that

are mutually dependent (e.g., Crespi 1992; Brown et al.

1997; Choe and Crespi 1997). Our perspective should

q22

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PROOF 12 The American Naturalist

Friday Mar 05 2004 01:46 PM/40103/der

compel evolutionary ecologists to incorporate physiolog-

ical mechanism more deeply into analyses of selection on

reproductive ecology (e.g., Shine and Guillette 1988; Shine

1995; Blackburn 2000), and physiologists should likewise

entertain the possibility that mechanisms represent more

or less maladaptive compromises rather than manifesta-

tions of optimized function subject to the particularities

of constraint. The forms of traits associated with viviparity,

matrotrophy, and placentation should be largely adaptive,

but the question becomes not just how but also for whom.

Acknowledgments

We are grateful to D. Haig, J. Joy, D. Lank, M. Loeb, P.

Nosil, J. Reynolds, R. Shine, J. Stewart, R. Trivers, T. Wil-

liams, K. Young, and D. Zeh for helpful discussions and

comments, and we thank the Natural Sciences and En-

gineering Research Council of Canada for ﬁnancial

support.

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Associate Editor: Allen J. Moore

q28

QUERIES TO THE AUTHOR

1 Please provide publication information for Aristotle’s

Historia Animalium to add this reference to the literature

cited.

2 Please see throughout manuscript: Parker 1995 is not

listed in the literature cited. Please provide reference in-

formation or delete from text.

3 See query 2

4 Please provide a citation for Haig in the sentence that

begins “As described by Haig ...”

5 Please provide a page number for direct citation of

the quote from Mossman 1937.

6 Please note: Throughout the manuscript, you seem

to go back and forth between using the past tense (here,

“Hamlett noted”) and the present tense (later, “Koob and

Callard provide”). I wanted to bring this to your attention.

It is not required that you are consistent one way or the

other, except maybe when a shift occurs in the same sen-

tence. Please review throughout.

7 Shine and Bull 1978 is not listed in the literature cited.

Did you intend to cite Shine and Bull 1979? If not, please

provide reference information or delete from text.

8 Please provide a page number for citation of the direct

quote from Wourms et al. 1988.

9 Haig 1991 is not listed in the literature cited. Did you

intend to cite some other Haig reference? If not, please

provide reference information or delete from text.

10 In the sentence that begins “Hemochorial placen-

tation ...,” would it be OK to change “given rise to an

endotheliochorial form” to “giving rise to ...”? This phras-

ing seems a bit unclear as is.

11 Please provide a page number for citation of the

direct quote from Blackburn et al. 1985.

12 Please provide a page number for citation of the

direct quote from Carter 2001.

13 Who are “They” in “They stated that ...”? Are you

referring again to Carter? Also, please provide a citation

and a page number for citation of the direct quote.

14 Please provide a page number for citation of the

direct quote from Pijnenborg et al. 1981.

15 Pijnenborg et al. 1995 is not listed in the literature

cited. Did you intend to cite Pijnenborg et al. 1985? If not,

please provide reference information or delete from text.

16 Please see throughout manuscript: Allen and Stewart

2001 is not listed in the literature cited. Please provide

reference information or delete from text.

17 See query 16

18 See query 16

19 See query 16

20 See query 16

21 Does the direct quote beginning “inverted yolk sacs

...” come from Mossman 1987? I moved it closer to the

quoted material, which is our style.

22 In the quote from Mossman that begins “Alternative

Hypotheses,” is it OK that I changed the brackets around

“for the evolution of placental diversity” to parentheses?

Do the brackets appear in how the text was originally

published?

23 Is it OK that I changed the hyphen in “morpholog-

ical-physiological starting points” to “and”?

24 In Carter and Han 1999, please spell out IGF in the

journal title.

25 Please verify that W. C. Hamlett was the author of

the 1999 reference “Placental and analogs in

elasmobranchs.”

26 Qualls and Shine 1998a is not cited in the text. Please

provide a citation or delete from literature cited.

27 Is the spelling of the second author’s name Prasad

or Prashad?

28 Please verify the spelling of the author’s last name

for Xavier et al. 1988. Is it Xavire or Xavier?

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Matrotrophy and polyandry partially regulate postcopulatory mechanisms and sexual selection in a bimodal viviparous salamander

Article

May 2024

The evolution of matrotrophic viviparity creates new scenarios within which evolutionary processes can operate, including postcopulatory events, family conflicts, and selective processes, which are expected to intensify with polyandry. We evaluated the effect of matrotrophic viviparity and polyandry on the reproductive output and offspring fitness of a bimodal reproductive vertebrate, the fire salamander (Salamandra salamandra), which presents two forms of viviparity: larviparity (i.e. females deliver many aquatic larvae) and pueriparity (i.e. females deliver a few terrestrial juveniles). Polyandry is present in both strategies, but matrotrophy only occurs in pueriparity. Analyses of paternity and offspring life-history traits in 18 pueriparous and 13 larviparous mother–offspring arrays suggest the presence of sibling conflicts in pueriparous salamanders, especially with polyandry. However, these postcopulatory processes did not increase reproductive skew in the pueriparous strategy compared to the larviparous one or lead to fitness differences across sires within a clutch, suggesting other selective processes operating earlier in the reproductive sequence. Observed male–female pairs were found to be genetically more similar than other potential pairings, although no relationship between males’ genetic traits and reproductive success was detected. This work advances our understanding of how sibling conflicts and sexual selection affect the evolution of viviparous matrotrophy and mating strategies.

Evidence for gene flow and trait reversal during radiation of Mexican Goodeid fish

Article

Full-text available

Jun 2024

Understanding the phylogeographic history of a group and identifying the factors contributing to speciation is an important challenge in evolutionary biology. The Goodeinae are a group of live-bearing fishes endemic to Mexico. Here, we develop genomic resources for species within the Goodeinae and use phylogenomic approaches to characterise their evolutionary history. We sequenced, assembled and annotated the genomes of four Goodeinae species, including Ataeniobius toweri , the only matrotrophic live-bearing fish without a trophotaenia in the group. We estimated timings of species divergence and examined the extent and timing of introgression between the species to assess if this may have occurred during an early radiation, or in more recent episodes of secondary contact. We used branch-site models to detect genome-wide positive selection across Goodeinae , and we specifically asked whether this differs in A. toweri , where loss of placental viviparity has recently occurred. We found evidence of gene flow between geographically isolated species, suggesting vicariant speciation was supplemented by limited post-speciation gene flow, and gene flow may explain previous uncertainties about Goodeid phylogeny. Genes under positive selection in the group are likely to be associated with the switch to live-bearing. Overall, our studies suggest that both volcanism-driven vicariance and changes in reproductive mode influenced radiation in the Goodeinae .

The roles of gene duplications in the dynamics of evolutionary conflicts

Article

Full-text available

Jun 2024
Proc Biol Sci

Evolutionary conflicts occur when there is antagonistic selection between different individuals of the same or different species, life stages or between levels of biological organization. Remarkably, conflicts can occur within species or within genomes. In the dynamics of evolutionary conflicts, gene duplications can play a major role because they can bring very specific changes to the genome: changes in protein dose, the generation of novel paralogues with different functions or expression patterns or the evolution of small antisense RNAs. As we describe here, by having those effects, gene duplication might spark evolutionary conflict or fuel arms race dynamics that takes place during conflicts. Interestingly, gene duplication can also contribute to the resolution of a within-locus evolutionary conflict by partitioning the functions of the gene that is under an evolutionary trade-off. In this review, we focus on intraspecific conflicts, including sexual conflict and illustrate the various roles of gene duplications with a compilation of examples. These examples reveal the level of complexity and the differences in the patterns of gene duplications within genomes under different conflicts. These examples also reveal the gene ontologies involved in conflict and the genomic location of the elements of the conflict. The examples provide a blueprint for the direct study of these conflicts or the exploration of the presence of similar conflicts in other lineages.

Species-Specific Seasonal Shifts in Reproductive Allocation in the Southern Grass Lizard, Takydromus sexlineatus (Lacertidae)

Article

Full-text available

Apr 2024

Simple Summary We designed a common garden experiment to collect data on female reproductive traits from three populations of Takydromus sexlineatus, testing the hypothesis that geographically separated populations should share a species-specific pattern of seasonal shifts in reproductive allocation. Six traits differed among populations, with four of the six also differing among successive clutches. Females grew longer during the breeding season and produced more eggs in the first clutch than in the subsequent clutches; egg size was unchanged throughout the breeding season. After removing the influence of female size or postpartum mass we found that (1) postpartum body mass, clutch mass, and relative clutch mass were greater in the Wuzhishan population than in the Shaoguan and Zhaoqing populations; (2) egg size was greatest in the Wuzhishan population and smallest in the Zhaoqing population; and (3) clutch size was greatest in the Wuzhishan population and smallest in the Shaoguan population. Our data validate the hypothesis tested. Abstract We designed a common garden design to collect data on female reproductive traits from three populations of the southern grass lizard Takydromus sexlineatus, testing the hypothesis that a species-specific pattern of seasonal shifts in reproductive allocation should be shared by geographically separated populations. Of the seven examined traits, six differed among populations, with four of the six also differing among successive clutches. Females grew longer during the breeding season and produced more eggs in the first clutch than in the subsequent clutches; egg size was unchanged throughout the breeding season. After removing the influence of female size or postpartum body mass we found the following. First, postpartum body mass, clutch mass, and relative clutch mass were greater in the Wuzhishan population than in the Shaoguan and Zhaoqing populations. Second, egg size was greatest in the Wuzhishan population and smallest in the Zhaoqing population. Third, clutch size was greatest in the Wuzhishan population and smallest in the Shaoguan population. Females did not trade-off egg size against number within each population × clutch combination. Our study validates the hypothesis tested, supports the conventional view that reproductive output is highly linked to maternal body size in lizards, and follows the classic prediction that females with different amounts of resources to invest in reproduction should give priority to adjusting the total number rather than size of their offspring.

Reconsidering the developmental origins of adult disease paradigm: The 'metabolic coordination of childbirth' hypothesis

Article

Full-text available

Jan 2024

In uncomplicated pregnancies, birthweight is inversely associated with adult non-communicable disease (NCD) risk. One proposed mechanism is maternal malnutrition during pregnancy. Another explanation is that shared genes link birthweight with NCDs. Both hypotheses are supported, but evolutionary perspectives address only the environmental pathway. We propose that genetic and environmental associations of birthweight with NCD risk reflect coordinated regulatory systems between mother and fetus, that evolved to reduce risks of obstructed labour. First, the fetus must tailor its growth to maternal metabolic signals, as it cannot predict the size of the birth canal from its own genome. Second, we predict that maternal alleles that promote placental nutrient supply have been selected to constrain fetal growth and gestation length when fetally expressed. Conversely, maternal alleles that increase birth canal size have been selected to promote fetal growth and gestation when fetally expressed. Evidence supports these hypotheses. These regulatory mechanisms may have undergone powerful selection as hominin neonates evolved larger size and encephalisation, since every mother is at risk of gestating a baby excessive for her pelvis. Our perspective can explain the inverse association of birthweight with NCD risk across most of the birthweight range: any constraint of birthweight, through plastic or genetic mechanisms, may reduce the capacity for homeostasis and increase NCD susceptibility. However, maternal obesity and diabetes can overwhelm this coordination system, challenging vaginal delivery while increasing offspring NCD risk. We argue that selection on viable vaginal delivery played an over-arching role in shaping the association of birthweight with NCD risk.

Evolutionary paths to new phenotypes

Article

Jan 2024
SCIENCE

Kathryn R. Elmer

Ecological model systems inform on innovative traits in plants and animals

Placental evolution from a three-dimensional and multiscale structural perspective

Article

Full-text available

Nov 2023
EVOLUTION

The placenta mediates physiological exchange between the mother and fetus. In placental mammals, all placentas are descended from a single common ancestor and functions are conserved across species; however, the placenta exhibits radical structural diversity. The selective pressures behind this structural diversity are poorly understood. Traditionally, placental structures have largely been investigated by grouping them into qualitative categories. Assessing the placenta on this basis could be problematic when inferring the relative ‘efficiency’ of a placental configuration to transfer nutrients from mother to fetus. We argue that only by considering placentas as 3D biological structures, integrated across scales, can the evolutionary questions behind their enormous structural diversity be quantitatively determined. We review the current state of placental evolution from a structural perspective, detail where 3D imaging and computational modelling have been used to gain insight into placental function, and outline an experimental roadmap to answer evolutionary questions from a multiscale 3D structural perspective. Our approach aims to shed light on placental evolution, and can be transferred to evolutionary investigations in any organ system.

Placentation and early primate development

Chapter

Jan 2024

Friderun Ankel-Simons

Siblicide

Chapter

May 2022

Andrew Goldklank Fulmer

Recent evolution of large offspring size and post-fertilization nutrient provisioning in swordtails

Preprint

Full-text available

Dec 2023

How organisms adapt to diverse environments is a foundational question in evolutionary biology. In addition to directly adapting to ecological conditions, organisms have evolved diverse reproductive strategies that impact the probability that their offspring survive to adulthood. Here, we describe divergence in reproductive strategy between two closely-related species of swordtail fish (Xiphophorus). Swordtail fish and their relatives have evolved viviparity: they have internal fertilization and give birth to fully developed fry. We find that one species, X. malinche, which lives in high-elevation environments, has evolved larger offspring than its closest relative X. birchmanni and dwarfs the offspring size of other species in the genus. The larger fry of X. malinche are more resilient to starvation than their X. birchmanni relatives, hinting that the evolution of large offspring size may be an adaptation to the particularly challenging environments in which X. malinche are born. We find that X. malinche achieves larger offspring size in part by continuing to provision their offspring over the course of embryonic development after fertilization, the first time this process has been documented in the Xiphophorus genus. Moreover, we observe differential regulation in the ovary of genes associated with post-fertilization nutrient provisioning in other species that use this reproductive strategy. These reproductive differences may drive an asymmetric hybrid incompatibility, since X. birchmanni mothers pregnant with F1 embryos give birth to premature and stillborn fry at an exceptionally high rate.

Embryonic Signals and Maternal Recognition

Chapter

Full-text available

Jan 1981

In the first paper of this volume Professor Amoroso argues that viviparity is a reproductive stratagem that has evolved many times in widely separated taxonomic groups of the animal kingdom. Retention of embryos within the body and the birth of living young occurs among representatives of all classes of vertebrates except birds, and in many groups of invertebrates. In the light of this wide distribution it is not surprising that solutions to problems posed by this evolutionary innovation are numerous (Amoroso et al., 1979). In eutherian and marsupial mammals, in which viviparity has become the preferred mode of reproduction, a prominent role has emerged for the corpus luteum. Progesterone secretion by the corpus luteum is essential for the establishment of gestation in all eutherians so far studied, and mechanisms have evolved that result in converting the female reproductive system from a cyclic pattern, in which oscillations of progesterone and estrogen secretion occur, to a noncyclic pattern, in which progesterone secretion is dominant. The time in gestation when this transformation occurs is an early indication of the maternal recognition of pregnancy (Short, 1969), and recent studies have focused on the nature of embryonic factors that signal this event (Heap and Perry, 1977).

Why do females mate multiply? A review of the genetic benefits

Article

Full-text available

Jan 2007

The aim of this review is to consider the potential benefits that females may gain from mating more than once in a single reproductive cycle. The relationship between non-genetic and genetic benefits is briefly explored. We suggest that multiple mating for purely non-genetic benefits is unlikely as it invariably leads to the possibility of genetic benefits as well. We begin by briefly reviewing the main models for genetic benefits to mate choice, and the supporting evidence that choice can increase offspring performance and the sexual attractiveness of sons. We then explain how multiple matin!: can elevate offspring fitness by increasing the number of potential sires that compete, when this occurs in conjunction with mechanisms of paternity biasing that function in copula or post-copulation. We begin by identifying cases where females use precopulatory cues to identify mates prior to remating. In the simplest case, females remate because they identify a superior mate and 'trade up' genetically. The main evidence for this process comes from extra-pair copulation in birds. Second, we note other cases where pre-copulatory cues may be less reliable and females mate with several males to promote post-copulatory mechanisms that bias paternity. Although a distinction is drawn between sperm competition and cryptic female choice, we point out that the genetic benefits to polyandry in terms of producing more viable or sexually attractive offspring do not depend on the exact mechanism that leads to biased paternity. Post-copulatory mechanisms of paternity biasing may: (1) reduce genetic incompatibility between male and female genetic contributions to offspring; (2) increase offspring viability if there is a positive correlation between traits favoured post-copulation and those that improve performance under natural selection; (3) increase the ability of sons to gain paternity when they mate with polyandrous females. A third possibility is that genetic diversity among offspring is directly favoured. This can be due to bet-hedging (due to mate assessment errors or temporal fluctuations in the environment), beneficial interactions between less related siblings of the opportunity to preferentially fertilise eggs with sperm of a specific genotype drawn from a range of stored sperm depending on prevailing environmental conditions. We use case studies from the social insects to provide some concrete examples of the role of genetic diversity among progeny in elevating fitness. We conclude that post-copulatory mechanisms provide a more reliable way of selecting a genetically compatible mate than pre-copulatory mate choice. Some of the best evidence for cryptic female choice by sperm selection is due to selection of more compatible sperm. Two future areas of research seem likely to be profitable. First, more experimental evidence is needed demonstrating that multiple mating increases offspring fitness via genetic gains. Second, the role of multiple mating in promoting assortative fertilization and increasing reproductive isolation between populations may help us to understand sympatric speciation.

THE EVOLUTION OF OVIPARITY WITH EGG GUARDING AND VIVIPARITY IN LIZARDS AND SNAKES: A PHYLOGENETIC ANALYSIS

Article

Feb 1996
EVOLUTION

This paper investigates the evolution of viviparity and of egg guarding in lizards and snakes in which three modes of reproduction can be described: oviparity without egg guarding, oviparity with egg guarding, and viviparity. All possible transitions of reproductive modes were detected in each taxon using Maddison's method. We then tested two specific hypotheses. First, egg guarding can be regarded as an alternative to viviparity. A relatively frequent association of egg guarding and viviparous species in the same taxon may be due to similar environmental conditions or species characteristics leading to two different solutions. Second, egg guarding may facilitate the evolution of viviparity. This hypothesis is supported by the high frequency of viviparous species in taxa containing egg guarding species and by a tendency for prolonged uterine retention of eggs in brooding squamates. Our analyses demonstrate that the first hypothesis is the best supported. Egg guarding and viviparity most often evolved independently. If a major benefit of egg guarding is the repulsion of potential predators, size is one of the most obvious morphological characters that should be correlated with the evolution of reproductive modes. The two reproductive traits were correlated to a reduction in body size for viviparous species and an increase in body size for egg guarding species. This could partly explain why the evolution of these reproductive modes seems almost antagonist.

ON IRREVERSIBLE EVOLUTION

Article

Sep 1985
EVOLUTION

REPTILIAN VIVIPARITY AND DOLLO'S LAW

Article

Oct 1998
EVOLUTION

It has been suggested repeatedly that the evolutionary transition from oviparity (egg-laying) to viviparity (live-bearing) in reptiles is irreversible. However, these adaptive arguments have yet to be tested by detailed examination of the phylogenetic distribution of oviparity and viviparity across a broad range of taxa. Using available data on reproductive modes and phylogenetic relationships within reptiles, we here quantify the numbers and directions of evolutionary transitions between oviparity and viviparity. Phylogenetic relationships among three diverse squamate groups (scincid lizards, colubrid snakes, elapid snakes) are currently inadequately known for inclusion in this study Among the remaining reptiles, oviparity has given rise to viviparity at least 35 times. Five possible instances of reversals (from viviparity to oviparity) are identified, but closer examination indicates that all have weak empirical support (i.e., they could be "unreversed" with little loss in parsimony, and/or are based on poorly substantiated phylogenetic hypotheses). Viviparity is clearly more frequently (and presumably easily) gained than lost in several disparate groups so far examined (reptiles, fishes, polychaete worms); this evolutionary bias should be considered when reproductive mode is optimized on a phylogeny or employed in phylogenetic reconstruction.

The evolution of viviparity in reptiles: an ecological analysis

Article

Jan 1985

Richard Shine

An ecological comparison of marsupial and placental patterns of reproduction

Chapter

Jan 1977

Pamela Parker

The traditional view of the relationship of marsupials is that of Huxley (1880), who held that Metatheria represent a stage of evolutionary development between the Prototheria (for example, platypus and spiny anteater) and the Eutheria (placental mammals). Huxley’s view implies that the living mammals thus represent three groups which evolved one from another, in the sequence Prototheria — Metatheria — Eutheria. It is this background against which features of marsupial anatomy and physiology may be interpreted as primitive in comparison with placental equivalents; thus several authors (for example, Lillegraven, 1969; Sharman, 1970) see certain aspects of marsupial reproductive biology as primitive, restrictive or inefficient when compared with similar features of placental reproduction.

1 The Maternal-Embryonic Relationship in Viviparous Fishes

Article

Dec 1988
Fish Physiol

This chapter discusses the maternal–embryonic relationship in viviparous fishes. Viviparity is a highly successful mode of reproduction that has evolved independently many times and with many variations in widely separated taxonomic groups. It occurs in all classes of vertebrates, except birds, and among many different groups of invertebrates. Initial steps in the evolution of viviparity involved a shift from external to internal fertilization and the retention of fertilized eggs in the female reproductive system. The osmoregulation of early embryos can be accomplished more efficiently and with less expenditure of embryonic energy in a maternally controlled uterine environment, but as development progresses to term, the embryos presumably acquire an increasing degree of osmoregulatory independence. Available evidence suggests that maternal regulation of the osmotic and chemical environment of the embryo also confers a selective advantage on viviparous teleosts. The uterine wall of most viviparous elasmobranchs and the coelocanth both delimits and defines the embryonic environment. The most spectacular maternal specializations for uterine gestation involve the uterine wall and involve (1) the amplification of the surface area in the form of folds, villi, or trophonemata; (2) the production of histotrophe or uterine milk’ (3) the compartmentalization of embryos; and (4) the development of placental attachment sites.

Reproductive biology of lamnoid sharks

Chapter

Jan 1993

Richard Grant Gilmore

The capture of recently inseminated or pregnant specimens of Carcharias taurus, Isurus paucus, I. oxyrinchus, Alopias superciliosus and A. vulpinus has allowed new information to be obtained on the reproductive biology of these species. Oophagy and embryonic cannibalism (adelphophagy) have been documented in C. taurus, but only oophagy in other lamnoid species. The occurrence of up to nine embryos of similar size per uterus in Isurus and no indication of functional erect teeth in embryos leaves considerable doubt that embryophagy occurs in this genus. Considerable data has been collected on Carcharias taurus which allows a lamnoid reproductive model to be developed and tested, in spite of the obvious differences between the reproductive biology of this species and other lamnoids. Gonad structure, ovarian development, fertilization, early embryonic differentiation, embryonic nutrition and parturition, in C. taurus and other lamnoids differs significantly from other elasmobranchs.

On the occurrence of oviparous and viviparous forms of the Mexican lizard Sceloporus aeneus

Article

Jan 1981
HERPETOLOGICA

L. J. Jr Guillette

Sceloporus aeneus, found at high elevations in southern Mexico, is reproductively biomodal with some populations exhibiting oviparity, others viviparity. Oviparity is exhibited by individuals in S. aeneus, whereas viviparity is exhibited by S. bicanthalis. Egg retention occurs in all females exhibiting oviparity. Egg retention is argued to be an intermediate stage in the evolution of viviparity. -from Author

Parent‐Offspring Conflict in the Evolution of Vertebrate Reproductive Mode

Abstract

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