ArticlePDF Available

Species phylogenetic relatedness, priority effects, and ecosystem functioning

Ecology

May 2012
93(5):1164-72

DOI:10.2307/23213510

Source
PubMed

Authors:

Jiaqi Tan

University of Pittsburgh

Zhichao Pu

Georgia Institute of Technology

Wade Alan Ryberg

Texas A&M University

Lin Jiang

Georgia Institute of Technology

Species immigration history can structure ecological communities through priority effects, which are often mediated by competition. As competition tends to be stronger between species with more similar niches, we hypothesize that species phylogenetic relatedness, under niche conservatism, may be a reasonable surrogate of niche similarity between species, and thus influence the strength of priority effects. We tested this hypothesis using a laboratory microcosm experiment in which we established bacterial species pools with different levels of phylogenetic relatedness and manipulated the immigration history of species from each pool into microcosms. Our results showed that strong priority effects, and hence multiple community states, only emerged for the species pool with the greatest phylogenetic relatedness. Community assembly also resulted in a significant positive relationship between bacterial phylogenetic diversity and ecosystem functions. Interestingly, these results emerged despite a lack of phylogenetic conservatism for most of the bacterial functional traits considered. Our results highlight the utility of phylogenetic information for understanding the structure and functioning of ecological communities, even when phylogenetically conserved functional traits are not identified or measured.

(a) Phylogeny based on Bayesian methods and (b) functional dendrogram based on cluster analysis (via unweighted pair group method with arithmetic mean [UPGMA]) of 57 traits for the study bacteria. Four species pools, Serratia (initial phylogenetic diversity [PD], 0.0065; initial functional richness [FR], 36; initial functional diversity [FD], 2.645), Staphylococcus (initial PD, 0.0274; initial FR, 42; initial FD, 7.224), Bacillus (initial PD, 0.0959; initial FR, 35; initial FD, 6.959), and the mixed-species pool (initial PD, 0.4854; initial FR, 50; initial FD, 7.550) were formed by these bacteria. Daggers indicate the bacteria constituting the mixed species pool. The scales for branch lengths are shown beneath the phylogenetic tree (panel a) and the functional dendrogram (panel b).

…

The b diversity among communities assembled from the four species pools with varying phylogenetic relatedness; b diversity is calculated as 1 À (Morisita similarity index). Values are means þ SE. Treatments sharing the same letters do not differ according to Tukey's HSD test.

…

Population density of each bacterium from the four species pools: (a) Serratia, (b) Staphylococcus, (c) Bacillus, and (d) mixed-species pool, at the end of the experiment. Values are means þ SE with density measured as colony formation units (CFU) per mL and was log 10 (x þ 1)-transformed prior to analysis.

…

Relationships between (a, b) realized phylogenetic diversity (PD), (c, d) functional richness (FR), (e, f ) functional diversity (FD) and (a, c, e) bacterial production and (b, d, f ) decomposition. PD and FD attained zero values in communities with one species. Data are plotted with linear regression lines. Bacterial production was measured as colony formation units (CFU) per mL and was log 10 (x þ 1)-transformed prior to analysis.

…

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Ecology, 93(5), 2012, pp. 1164– 1172

Ó2012 by the Ecological Society of America

Species phylogenetic relatedness, priority effects,

and ecosystem functioning

JIAQI TAN,

1,3

ZHICHAO PU,

WADE A. RYBERG,

1,2

AND LIN JIANG

School of Biology, Georgia Institute of Technology, 310 Ferst Drive, Atlanta, Georgia 30332 USA

Department of Wildlife and Fisheries Sciences, Texas A&M University, 210 Nagle Hall, College Station, Texas 77843 USA

Abstract. Species immigration history can structure ecological communities through

priority effects, which are often mediated by competition. As competition tends to be stronger

between species with more similar niches, we hypothesize that species phylogenetic relatedness,

under niche conservatism, may be a reasonable surrogate of niche similarity between species,

and thus inﬂuence the strength of priority effects. We tested this hypothesis using a laboratory

microcosm experiment in which we established bacterial species pools with different levels of

phylogenetic relatedness and manipulated the immigration history of species from each pool

into microcosms. Our results showed that strong priority effects, and hence multiple

community states, only emerged for the species pool with the greatest phylogenetic

relatedness. Community assembly also resulted in a signiﬁcant positive relationship between

bacterial phylogenetic diversity and ecosystem functions. Interestingly, these results emerged

despite a lack of phylogenetic conservatism for most of the bacterial functional traits

considered. Our results highlight the utility of phylogenetic information for understanding the

structure and functioning of ecological communities, even when phylogenetically conserved

functional traits are not identiﬁed or measured.

Key words: bacteria; community assembly; ecosystem function; multiple community states; phyloge-

netic relatedness; priority effects.

INTRODUCTION

Understanding mechanisms underlying the assembly

of ecological communities is one of the central goals of

community ecology (Gleason 1927, Diamond 1975).

Ecologists now recognize that both niche-based deter-

ministic processes (Chase and Leibold 2003) and neutral

stochastic processes (Bell 2001, Hubbell 2001) can

operate during the process of community assembly.

Niche-based processes involve the interaction between

species’ niches and the conditions of the environment

where they live, which can jointly regulate the structure

of the assembling communities. In habitats with similar

environmental conditions and under the same regional

species pool, such processes often result in convergent

communities with similar species composition and

abundance. Stochastic processes, highlighted by the

neutral theory (Bell 2001, Hubbell 2001), can also

strongly impact ecological communities. In particular,

stochasticity in the order and timing of species

colonization events, as demonstrated by both theoretical

and empirical studies (e.g., Drake 1991, Law and

Morton 1993, Jiang and Patel 2008, Fukami et al.

2010; reviewed by Chase 2003), can result in divergent

communities dominated by different species. These

multiple community states associated with different

species colonization histories frequently arise from

priority effects, in which early colonizing species affect

the establishment and abundance of later colonizers.

One factor that can potentially inﬂuence the relative

importance of deterministic and stochastic processes, and

hence the strength of priority effects, is ecological

similarity of species in the regional species pool. Both

theory (e.g., MacArthur and Levins 1967) and experi-

ments (e.g., Gause 1934) have demonstrated the difﬁculty

for species with similar niches to coexist, which prompted

Hardin (1960) to coin the competitive exclusion principle.

A corollary of this principle, applying to community

assembly, is that increasing ecological similarity of species

in the regional pool may make it more likely for species

already established at a locality to have strong negative

impacts on newly colonizing species, promoting inhibitive

priority effects. As species niches are often difﬁcult to

quantify and phylogenetically closely related species tend

to possess similar niches (i.e., phylogenetic niche conser-

vatism; Harvey and Pagel 1991, Prinzing et al. 2001,

Webb et al. 2002, Donoghue 2008), we suggest that

species phylogenetic relatedness may be used as a

surrogate of niche similarity to predict the strength of

competition and priority effects. The positive relationship

between species phylogenetic relatedness and competition

was in fact ﬁrst hypothesized by Darwin (1859), and

supported by a recent experiment (Violle et al. 2011).

However, whether phylogenetic relatedness of the region-

Manuscript received 24 August 2011; revised 28 November

2011; accepted 30 November 2011. Corresponding Editor: J. B.

Yavitt.

E-mail: jtan@gatech.edu

1164

al species pool inﬂuences the strength of priority effects

during community assembly remains an open question.

Phylogenetic relatedness of the regional species pool

may also have consequences for the functioning of the

assembled communities. For example, if phylogenetic

relatedness serves as a reasonable surrogate for species

ecological similarity, then low phylogenetic relatedness

(i.e., high phylogenetic diversity) may translate into

increased niche complementarity among species in the

assembled communities, potentially resulting in high

levels of ecosystem functioning (Cavender-Bares et al.

2009). On the other hand, high phylogenetic relatedness

among species within the regional species pool would

indicate possible redundancy in species’ niches, likely

leading to reduced ecosystem functioning. So far only a

handful of studies have investigated the relevance of

species phylogenetic relatedness for ecosystem function-

ing (Maherali and Klironomos 2007, Cadotte et al. 2008,

2009, Jiang et al. 2010), but the potential interactive

effects of phylogenetic relatedness and assembly history

on ecosystem functions have not been explored.

Here, we describe an experimental study examining

how species phylogenetic relatedness affects priority

effects and ecosystem functioning by using a laboratory

model of bacterial communities. We established bacte-

rial species pools with different levels of species

phylogenetic relatedness and manipulated the immigra-

tion history of bacteria from each species pool into the

assembled communities. We showed that signiﬁcant

dissimilarity among communities subjected to different

assembly histories emerged only when bacteria in the

species pool were phylogenetically closely related. We

also found signiﬁcant effects of phylogenetic relatedness

and assembly history on bacterial ecosystem functions

(i.e., bacterial production and decomposition).

MATERIAL AND METHODS

Our experiment used eight strains of common

environmental bacteria from freshwater ecosystems

(Fig. 1), all of which can form colonies with unique

morphological characteristics on agar plates. To esti-

mate phylogenetic relatedness between these bacteria,

we constructed phylogeny based on bacterial 16S rRNA

sequences (Fig. 1a). We sequenced the 16S rRNA gene

of each bacterial strain, aligned the sequences with

Clustal X (version 2.0; Larkin et al. 2007), selected the

best sequence evolution model, GTRþG with MrModel-

test (version 2.3; Nylander 2004), by using the Akaike

information criterion, and built the phylogenetic tree

with Bayesian method in MrBAYES (version 3.1.2;

Huelsenbeck and Ronquist 2001). Three archaea were

used as the out-group. The phylogenetic distance

between bacteria was obtained by summing lengths of

the intervening branches between the two species on the

phylogeny; smaller phylogenetic distance between bac-

teria indicates greater phylogenetic relatedness. Using

these eight strains of bacteria, we established four

species pools: Serratia,Staphylococcus,Bacillus, and a

mixed-genus pool with one bacterium randomly selected

from each of the single-genus pools (Fig. 1a; see Plate 1).

The phylogenetic diversity (hereafter PD) of each species

pool was calculated by summing the lengths of all the

intervening branches of all the species in each pool

(Faith 1992). PD is thus an aggregate measure of the

phylogenetic relatedness of each species pool; higher PD

values indicate larger phylogenetic distances and thus

weaker phylogenetic relatedness among species.

We estimated functional trait diversity of each species

pool based on the bacteria’s ability to utilize a variety of

carbon substrates that may appear in the bacterial

growth medium used in our experiment. We measured

55 bacterial traits with Biolog MicroPlates (Biolog,

Hayward, California, USA). Following the manufactur-

er’s instructions, we prepared and inoculated Gram-

positive and Gram-negative bacterial cultures into their

corresponding type of Biolog MicroPlates. Gram-

positive and Gram-negative microplates, each contain-

ing 96 wells, share 55 carbon substrates in common, so

we only recorded the results of these 55 traits. We scored

positive results, indicating that the species was able to

use carbon sources in the wells, as 1 and negative results

as 0. In addition, we tested the ability of these bacteria to

utilize two common carbon substrates: cellulose and

starch. We spread diluted cultures of each bacterial

strain on carboxymethylcellulose (Wohl et al. 2004) and

starch agar plates, incubated them at room temperature

(;228C) for 5 days, and ﬂooded plates with 1%Gango

Red and Lugol’s iodine solutions, respectively. Colorless

zones around bacterial colonies on agar plates were

observed if bacteria utilize cellulose or starch. Based on

the total 57 traits, we calculated functional trait diversity

of each species pool in two ways. First, we calculated

functional richness (hereafter FR) by counting the total

number of carbon substrates that bacteria from a species

pool could utilize. Second, we calculated functional

diversity (hereafter FD) of each species pool. We

performed a UPGMA-based cluster analysis (unweight-

ed pair group method with arithmetic mean) with the

Euclidean distance between bacteria in the 57-dimen-

sional trait space to produce the functional dendrogram

(Fig. 1b), and calculated FD of each species pool as the

total intervening branch lengths of all the species in the

pool on the dendrogram (Petchey and Gaston 2002). To

test for phylogenetic conservatism of the measured

traits, we conducted a Mantel test based on 10 000

permutations that evaluated the correlation between

bacterial phylogenetic distance and trait Euclidean

distance. We also tested the phylogenetic signal of each

trait with Blomberg’s K (Blomberg et al. 2003), using

the multiPhylosignal function in the Picante package

(Kimbel et al. 2010).

Our experiment used 25-mL capped test tubes as

microcosms, each of which contained 10 mL of medium.

The medium contained 0.55 g of crushed protozoan

pellets (Carolina Biological Supply, Burlington, North

Carolina, USA) per liter of deionized water. Protozoan

May 2012 1165PHYLOGENY AND COMMUNITY ASSEMBLY

pellets are made from grass and include a variety of

common carbon resources for bacterial growth. Medium

was autoclaved in large ﬂasks and ﬁltered to remove

insoluble particles, then transferred into experimental

microcosms and autoclaved again before the experiment

started. The microcosms were incubated on a shaker at

200 rpm under room temperature (;228C).

The experiment included all the possible assembly

sequences for each bacterial pool. Thus, we had two

sequential assembly history treatments for the Serratia

pool that contained two species, and six for the

Staphylococcus, Bacillus, and mixed pools that each

contained three species (Fig. 1). Each treatment was

replicated three times. Prior to the experiment, we

prepared stock cultures of each bacterial strain in 8%

nutrient broth. At the beginning of the experiment (day

0), we introduced the ﬁrst species into microcosms by

transferring a small volume (,5lL) of stock culture

with an aseptic loop. In the same way, on days 7 and 14,

we introduced the second and third immigrants (no third

immigrant for the Serratia communities), respectively.

The weekly interval between species introduction

allowed the assembled communities to equilibrate before

the next introduction event. Our pilot experiment, albeit

using only half of the eight bacterial strains used in this

study, indicated that bacterial populations of individual

species, initiated at small size in isolation from other

species, require 2–3 days to reach carrying capacity and

persist at the stationary phase for at least our

experimental duration; bacterial communities contain-

ing multiple species generally reach equilibrium in one

week and can persist for similarly long periods of time

(J. Tan, unpublished data). On day 21, we added a dried,

weighed, and autoclaved wheat seed to each microcosm.

On day 49, we terminated the experiment and destruc-

tively sampled the microcosms. The samples from

microcosms were serially diluted and spread on nutrient

agar plates. After 7-day incubation, we counted the

number of bacterial colonies on plates to determine

population density (colony formation units per milliliter

[CFU/mL]) of each bacterial strain. Wheat seeds were

retrieved from microcosms, oven dried, and weighed.

Two ecosystem functions were recorded. Total bacterial

production in each microcosm was obtained by sum-

ming the density of each bacterial strain. Decomposition

was measured as the fraction of wheat seed mass lost

during the experiment.

FIG. 1. (a) Phylogeny based on Bayesian methods and (b) functional dendrogram based on cluster analysis (via unweighted pair

group method with arithmetic mean [UPGMA]) of 57 traits for the study bacteria. Four species pools, Serratia (initial phylogenetic

diversity [PD], 0.0065; initial functional richness [FR], 36; initial functional diversity [FD], 2.645), Staphylococcus (initial PD,

0.0274; initial FR, 42; initial FD, 7.224), Bacillus (initial PD, 0.0959; initial FR, 35; initial FD, 6.959), and the mixed-species pool

(initial PD, 0.4854; initial FR, 50; initial FD, 7.550) were formed by these bacteria. Daggers indicate the bacteria constituting the

mixed species pool. The scales for branch lengths are shown beneath the phylogenetic tree (panel a) and the functional dendrogram

(panel b).

JIAQI TAN ET AL.1166 Ecology, Vol. 93, No. 5

We calculated realized community PD, FR, and FD,

based on the realized species composition measured at the

end of the experiment. We calculated bdiversity between

communities sharing the same species pool but subjected

to different assembly histories, by ﬁrst calculating the

modiﬁed Morisita similarity index (Horn 1966), then

subtracting it from 1. Calculation of Morisita indices was

based on untransformed bacterial density data. For

subsequent statistical analyses, all the bacteria density

data were log

-transformed (log

[xþ1]) to improve

normality. We used one-way ANOVA with bdiversity as

the dependent variable and species pool as the class

variable to assess the effect of varying phylogenetic

relatedness among species pools on history-induced

differences in community structure, as represented by b

diversity. Tukey’s HSD was further conducted as the post

hoc test. To test the effect of assembly history on the

density of bacteria in communities sharing the same

species pool, we used MANOVA with bacteria densities

for each species pool as the dependent variable and

history sequence as the class variable. To test the effect of

assembly history on bacterial production and decompo-

sition in different species pools, we used nested ANOVA

with production and decomposition as the dependent

variables and history sequences as a factor nested within

species pools. To further test the effect of assembly

history, we used one-way ANOVA within each species

pool, with production and decomposition as the depen-

dent variables and assembly history sequence as the

independent variable. To test the effect of phylogenetic

and functional diversity on bacterial production and

decomposition, we used simple and backward-selection

multiple linear regressions to model the ecosystem

functions (i.e., bacterial production and decomposition)

as functions of realized PD, FR, and FD. In all the

regressions, explanatory variables were deemed signiﬁ-

cant if P0.05.

RESULTS

Our study bacteria did not exhibit signiﬁcant phyloge-

netic conservatism when all the 57 traits were considered

together (Mantel test, P¼0.152). When examined

individually, 9 of 57 traits (15%), including D-fructose,

L-fucose, a-D-glucose, a-D-lactose, D-melibiose, D-

alanine, D, L, a-glycerol phosphate, a-D-glucose-1-phos-

phate, and D-glucose-6-phosphate, showed signiﬁcant

phylogenetic signals (multiPhylosignal function, P,

0.05).

The bdiversity among communities subjected to

different histories varied signiﬁcantly among the four

species pools (ANOVA, F

3, 411

¼443.081, P,0.001).

This signiﬁcant variation mainly resulted from the larger

values of bdiversity observed in the Serratia pool (see

Fig. 2; Tukey’s HSD). The dominant species in

communities of the Serratia pool differed depending

on history treatments (Fig. 3a). In contrast, in the

Staphylococcus,Bacillus, and mixed-species pools, the

dominant species remained the same in different history

treatments (Fig. 3b–d). Nevertheless, MANOVA still

revealed a signiﬁcant effect of assembly history on

species densities in those species pools (Staphylococcus,

Wilks’ lambda ¼0.010, F

15,28

¼7.882, P,0.001;

Bacillus, Wilks’ lambda ¼0.029, F

15,28

¼4.867, P,

0.001; mixed, Wilks’ lambda ¼0.018, F

15,28

¼6.097, P,

0.001), in addition to the signiﬁcant effect of history for

the Serratia pool (Wilks’ lambda ¼0.017, F

1,4

¼234.1, P

,0.001).

Nested ANOVA revealed a signiﬁcant effect of

assembly history on bacterial production (F

5,40

14.449, P,0.001), but no effect of assembly history

on decomposition (F

5,40

¼0.886, P¼0.499). One-way

ANOVA indicated that assembly history had a signif-

icant effect on bacterial production in communities of

the Staphylococcus (F

5,12

¼30.086, P,0.001), Bacillus

5,12

¼16.888, P,0.001), and mixed (F

5,12

¼3.601, P¼

0.032) pools, but had no effects in communities of the

Serratia pool (F

1,4

¼1.136, P¼0.346). In contrast,

assembly history signiﬁcantly affected decomposition in

the Staphylococcus communities only (Staphylococcus,

5,12

¼37.615, P,0.001; Serratia,F

1,4

¼1.136, P¼

0.346; Bacillus,F

5,12

¼0.670, P¼0.654; mixed, F

5,12

2.348, P¼0.105). Nested ANOVA also revealed that

ecosystem function level differed signiﬁcantly in com-

munities of different species pools (production, F

14,40

41.161, P,0.001; decomposition, F

14,40

¼6.288, P,

0.001).

Simple linear regressions showed that both bacterial

production and decomposition increased with realized

FIG. 2. The bdiversity among communities

assembled from the four species pools with

varying phylogenetic relatedness; bdiversity is

calculated as 1 (Morisita similarity index).

Values are means þSE. Treatments sharing the

same letters do not differ according to Tukey’s

HSD test.

May 2012 1167PHYLOGENY AND COMMUNITY ASSEMBLY

PD (Fig. 4a; R

¼0.461, P,0.001; Fig. 4b; R

¼0.212,

P,0.001), FR (Fig. 4c; R

¼0.586, P,0.001; Fig. 4d;

¼0.410, P,0.001), and FD (Fig. 4e; R

¼0.268, P

,0.001; Fig. 4f; R

¼0.415, P,0.001), respectively.

Multiple regression models retained realized FR and FD

as best predictors of both bacterial production and

decomposition.

DISCUSSION

The results of our experiment demonstrated the

importance of understanding species phylogenetic relat-

edness when predicting the strength of priority effects.

We observed the highest bdiversity among communities

in the Serratia pool (Fig. 2), which contained phyloge-

netically most closely related bacterial strains (Fig. 1a).

FIG. 3. Population density of each bacterium from the four species pools: (a) Serratia,(b)Staphylococcus, (c) Bacillus, and (d)

mixed-species pool, at the end of the experiment. Values are means þSE with density measured as colony formation units (CFU )

per mL and was log

(xþ1)-transformed prior to analysis.

JIAQI TAN ET AL.1168 Ecology, Vol. 93, No. 5

Different Serratia marcescens strains were dominant in

these communities when subjected to different assembly

histories (Fig. 3a). In contrast, communities from each

of the other pools with lower phylogenetic relatedness

were structurally similar (Fig. 2), containing the same

dominant species regardless of history (Fig. 3b–d). This

difference emerged despite the fact that history had a

signiﬁcant effect on the structure of the assembled

communities for all species pools, as revealed by

MANOVA. These results appear consistent with our

hypothesis that stronger competition may occur between

species that are more closely related phylogenetically

FIG. 4. Relationships between (a, b) realized phylogenetic diversity (PD), (c, d) functional richness (FR), (e, f ) functional

diversity (FD) and (a, c, e) bacterial production and (b, d, f) decomposition. PD and FD attained zero values in communities with

one species. Data are plotted with linear regression lines. Bacterial production was measured as colony formation units (CFU) per

mL and was log

(xþ1)-transformed prior to analysis.

May 2012 1169PHYLOGENY AND COMMUNITY ASSEMBLY

(Maherali and Klironomos 2007, Violle et al. 2011),

leading to stronger priority effects that generate multiple

community states (Chase and Leibold 2003, Fukami and

Lee 2006). However, phylogenetic conservatism was not

detected when all bacterial traits were considered

together, and nonsigniﬁcant phylogenetic signals were

detected for the majority of measured traits. At least

three mutually nonexclusive explanations can account

for these results. One possibility is that at least some of

the phylogenetically conserved traits that we measured

are important in deﬁning the ecological niches of our

study bacteria in our experiment. This is supported by

the fact that phylogenetic diversity and functional

diversity based on measured traits (including FR and

FD) were both positively related to bacterial production

and decomposition in our experiment. Another possi-

bility is that some unmeasured traits that are important

in deﬁning species niches may be phylogenetically

conserved, making phylogenetic relatedness a reason-

able proxy of functional similarity with regard to these

traits. A third explanation is that phylogenetic relation-

ships based on the 16S rRNA gene, which is known to

be highly conserved between different species of bacteria

(Coenye and Vandamme 2003), may not adequately

capture the potentially large variation in traits coded by

less conserved genes (see Dahle et al. 2011 for a

counterexample). Note that this issue can be circum-

vented in the future by constructing phylogeny based on

whole genomes, which are currently unavailable for

most organisms. Regardless, our results highlight the

utility of phylogenetic information for understanding

the structure and functioning of ecological communities,

even when phylogenetically conserved functional traits

are not identiﬁed or measured.

Our results indicated that phylogenetic diversity

positively affected ecosystem functions (i.e., bacterial

production and decomposition), but that ecosystem

functioning was better predicted by functional diversity.

Using data from plant experiments, Cadotte et al. (2008,

2009) also showed that primary productivity was

positively correlated with both plant phylogenetic and

functional diversity. However, their results indicated

that phylogenetic diversity explained more variation in

plant productivity than several measurements of func-

tional diversity. This discrepancy between the results of

the two studies may be due to the fact that horizontal

PLATE 1. Colonies of the eight bacteria studied, on agar plates. Photo credits: J. Tan and L. Jiang.

JIAQI TAN ET AL.1170 Ecology, Vol. 93, No. 5

gene transfer, which may increase trait similarity among

distantly related species and weaken the correlation

between phylogenetic relatedness and trait similarity, is

much more common for bacteria than for plants

(Andersson 2005, Richardson and Palmer 2007). Note

that phylogenetic diversity nevertheless remained signif-

icant in explaining the functioning of bacterial commu-

nities in our experiment.

Our results also showed that community assembly

history had signiﬁcant effects on bacterial production in

the Staphylococcus,Bacillus, and mixed communities,

and on decomposition in the Staphylococcus communi-

ties. Likewise, Fukami et al. (2010) manipulated the

assembly history of wood-decay fungal communities and

found a signiﬁcant effect of assembly history on fungal

decomposition. They showed that community diver-

gence in species richness and composition, resulting

from different assembly histories, led to the differenti-

ation of ecosystem functioning. However, this mecha-

nism cannot explain the divergence/convergence of

ecosystem functioning in communities subjected to

different assembly histories in our study. Two distinct

alternative states were formed in communities of the

Serratia pool (Fig. 3a), but ecosystem functions of these

two community states were similar. In contrast, a single

community state was observed in the Staphylococcus

pool, but ecosystem functions differed among the

assembled communities (Fig. 3b). One explanation for

the lack of historical effects on ecosystem functioning in

the Serratia communities is that the two strains of

Serratia marcescens may play similar ecological roles

since they are phylogenetically closely related (99%

similarity based on phylogeny) and functionally similar

(sharing 50 of 57 traits). The two Serratia strains may

thus be largely functionally substitutable, resulting in the

same levels of ecosystem functions in communities

dominated by different Serratia strains. In other species

pools, although the historical effect was not strong

enough to generate multiple community states, the

abundance of subdominant species differed under

different assembly histories (hence the signiﬁcant effect

of assembly history on species densities in MANOVA),

especially in the Staphylococcus pool (Fig. 3b), which

may have caused the differentiation of ecosystem

functioning in those species pools. All together, our

results showed that assembly history affected ecosystem

functioning in some communities, but not in others.

Understanding the conditions that promote the rela-

tionship between assembly history and ecosystem

functioning remains an important topic of future

research.

One concern is that each phylogenetic relatedness

level in our experiment included only one species

combination, so one could argue that the effect of

phylogenetic relatedness may have been confounded

with the effect of species identity. An ideal solution to

this problem would be to use as many species

combinations at each phylogenetic level as possible,

but this may not be logistically possible. In particular,

ﬁnding many combinations of phylogenetically closely

related bacteria with different colony morphologies

(e.g., the red and white Serratia marcescens) is difﬁcult.

In this experiment, although we cannot exclude the

possibility that the effects of species phylogenetic

relatedness and identity are confounded, results from a

related experiment suggests that this is not the case. That

experiment produced results similar to the current

experiment. In particular, strong priority effects were

also observed in bacterial communities containing

closely related species, speciﬁcally those with three

strains of Bacillus pumilus; weaker priority effects were

detected in communities with less related species (J. Tan,

unpublished data). In the present experiment, weak

priority effects also emerged in all communities of the

three species pools with relatively low levels of

phylogenetic relatedness, resulting in single community

states. Together, these results strongly suggest a linkage

between species phylogenetic relatedness and the

strength of priority effects. Nevertheless, future studies

that manipulate phylogenetic relatedness or diversity

should aim to establish multiple species combinations

within each treatment, in order to eliminate the potential

confounding effects from species identity.

In this study, different bacterial species pools exhib-

ited different levels of phylogenetic relatedness, permit-

ting an evaluation of how phylogenetic relatedness

might govern the relative contributions of niche-based

deterministic processes (Chase and Leibold 2003) and

neutral stochastic processes (Bell 2001, Hubbell 2001) to

community assembly. In the experiment we conducted

to accomplish this evaluation, multiple community

states resulting from strong stochastic assembly pro-

cesses (i.e., priority effects) were only observed in the

species pool with the highest phylogenetic relatedness

and highest functional similarity. Alternatively, single-

community states resulting from strong deterministic

assembly processes were observed in communities

assembled from less phylogenetically related species

pools. As such, these observations support our hypoth-

esis that priority effects are stronger between species that

are more closely related phylogenetically, although some

caution must be exercised when generalizing these

results given the limitation of our experimental design

(see last paragraph). Further, our study demonstrates a

positive relationship between phylogenetic diversity and

ecosystem functions in an experiment that directly

manipulated phylogenetic diversity. Importantly, we

obtained these results despite the fact that many

functional traits measured in our experiment exhibited

nonsigniﬁcant phylogenetic signals. Our results thus

highlight the difﬁculty of identifying species functional

traits relevant for community assembly and ecosystem

functioning, and at the same time, the utility of basic

phylogenetic information in predicting the structure and

functioning of ecological communities.

May 2012 1171PHYLOGENY AND COMMUNITY ASSEMBLY

ACKNOWLEDGMENTS

We thank Michael Cortez, Cyrille Violle, Edward Burdette,

and two anonymous reviewers for their insightful comments,

which improved the manuscript. This project was supported by

a British Ecological Society early career project grant and U.S.

NSF grant (DEB-1120281) awarded to L. Jiang.

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JIAQI TAN ET AL.1172 Ecology, Vol. 93, No. 5

Bridging theory and experiments of priority effects

Article

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TRENDS ECOL EVOL

Priority effects play a key role in structuring natural communities, but considerable confusion remains about how they affect different ecological systems. Synthesizing previous studies, we show that this confusion arises because the mechanisms driving priority and the temporal scale at which they operate differ among studies, leading to divergent outcomes in species interactions and biodiversity patterns. We suggest grouping priority effects into two functional categories based on their mechanisms: frequency-dependent priority effects that arise from positive frequency dependence, and trait-dependent priority effects that arise from time-dependent changes in interacting traits. Through easy quantification of these categories from experiments, we can construct community models representing diverse biological mechanisms and interactions with priority effects, therefore better predicting their consequences across ecosystems.

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Interactions among parasites and other microbes within hosts can impact disease progression, yet study of such interactions has been mostly limited to pairwise combinations of microbes. Given the diversity of microbes within hosts, indirect interactions among more than two microbial species may also impact disease. To test this hypothesis, we performed inoculation experiments that investigated interactions among two fungal parasites, Rhizoctonia solani and Colletotrichum cereale, and a systemic fungal endophyte, Epichloë coenophiala, within the grass, tall fescue (Lolium arundinaceum). Both direct and indirect interactions impacted disease progression. While the endophyte did not directly influence R. solani disease progression or C. cereale symptom development, the endophyte modified the interaction between the two parasites. The magnitude of the facilitative effect of C. cereale on the growth of R. solani tended to be greater when the endophyte was present. Moreover, this interaction modification strongly affected leaf mortality. For plants lacking the endophyte, parasite co-inoculation did not increase leaf mortality compared to single-parasite inoculations. By contrast, for endophyte-infected plants, parasite co-inoculation increased leaf mortality compared to inoculation with R. solani or C. cereale alone by 1.9 or 4.9 times, respectively. Together, these results show that disease progression can be strongly impacted by indirect interactions among microbial symbionts.

Microhabitats Shape Bacterial Community Composition, Ecosystem Function, and Genome Traits

Thesis

Jan 2018

Marian Schmidt

This dissertation helps to integrate bacteria into the broader field of ecology by investigating bacterial community composition and diversity as it relates to ecosystem function in microhabitats within freshwater systems of the Great Lakes Region. Here, I combine field- and laboratory-based measurements of observational data collected from three major types of lake ecosystems: inland lakes, a freshwater estuary (Muskegon Lake), and a Great Lake (Lake Michigan). First, to determine the primary controls on lake bacterial community composition, I assessed the influence of lake layer (i.e. stratification), lake productivity, and particle-association on the bacterial community across 11 inland lakes with varying productivity in Southwestern Michigan. I found that particle-association very strongly structures freshwater bacterial community composition. Second, I studied a freshwater estuarine lake, Muskegon Lake, which has a large spatio-temporal variation in bacterial heterotrophic productivity, to test whether there was an association between heterotrophic production and bacterial biodiversity (defined as the number of taxa and taxon abundance). I specifically focused on two co-occurring freshwater habitats that my first chapter showed to be populated by very distinct communities: particle-associated and free-living. Positive biodiversity-heterotrophic productivity relationships were found only in particles. Third, I performed a genome-based analysis of free-living specialists, particle-associated bacterial specialists, and generalists to characterize the genomic architecture and genetic traits that are associated with adaptations to these specific habitats. The genomes of particle-associated specialist bacteria were about twice the size of the genomes of free-living specialists and generalists, which had streamlined genomes. Fourth, to identify the bacterial taxa driving heterotrophic productivity across the large set of lake samples, I found that high nucleic acid (i.e., HNA) functional groups identified by flow cytometry can serve as a proxy for freshwater bacterial heterotrophic productivity, whereas low nucleic acid (i.e., LNA) functional groups cannot. Then, I used a machine learning approach to identify bacterial taxa associated with HNA and LNA. This allowed me to identify the bacterial taxa, which were often members of the Phylum Bacteroidetes, that are associated heterotrophic productivity. Finally, I investigated patterns of lake specificity and phylogenetic conservation of taxonomic groups. Throughout my dissertation, I found that there was very deep (Class to Phylum-level) phylogenetic conservation of which bacteria lived in which habitats, but not of what bacterial taxa contributed to HNA and LNA functional groups, and thus heterotrophic productivity. Positive biodiversity-heterotrophic productivity relationships only existed in particle-associated, and not free-living communities, and communities composed of more phylogenetically related organisms were more productive per-capita. These differences in biodiversity-ecosystem function relationships may in part be explained by particle-associated bacteria having larger genomes, higher nitrogen content, and more unique genes that provide the potential for niche complementarity. The taxa that drove HNA and LNA cell numbers, and by proxy heterotrophic productivity, were lake and time-specific and indicated that taxa could switch between the two functional groups. Overall, my dissertation elucidates the ecological and evolutionary effects of microhabitat structure on bacterial communities and genomes in natural systems.

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Composition, function, and timing: exploring the early-life gut microbiota in piglets for probiotic interventions

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Background The establishment of a robust gut microbiota in piglets during their early developmental stage holds the potential for long-term advantageous effects. However, the optimal timeframe for introducing probiotics to achieve this outcome remains uncertain. Results In the context of this investigation, we conducted a longitudinal assessment of the fecal microbiota of 63 piglets at three distinct pre-weaning time points. Simultaneously, we gathered vaginal and fecal samples from 23 sows. Employing 16S rRNA gene and metagenomic sequencing methodologies, we conducted a comprehensive analysis of the fluctuation patterns in microbial composition, functional capacity, interaction networks, and colonization resistance within the gut microbiota of piglets. As the piglets progressed in age, discernible modifications in intestinal microbial diversity, composition, and function were observed. A source-tracking analysis unveiled the pivotal role of fecal and vaginal microbiota derived from sows in populating the gut microbiota of neonatal piglets. By D21, the microbial interaction network displayed a more concise and efficient configuration, accompanied by enhanced colonization resistance relative to the other two time points. Moreover, we identified three strains of Ruminococcus sp. at D10 as potential candidates for improving piglets' weight gain during the weaning phase. Conclusions The findings of this study propose that D10 represents the most opportune juncture for the introduction of external probiotic interventions during the early stages of piglet development. This investigation augments our comprehension of the microbiota dynamics in early-life of piglets and offers valuable insights for guiding forthcoming probiotic interventions.

Fungal Fight Club: phylogeny and growth rate predict competitive outcomes among ectomycorrhizal fungi

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FEMS MICROBIOL ECOL

Ectomycorrhizal fungi are among the most prevalent fungal partners of plants and can constitute up to one-third of forest microbial biomass. As mutualistic partners that supply nutrients, water, and pathogen defense, these fungi impact host plant health and biogeochemical cycling. Ectomycorrhizal fungi are also extremely diverse, and the community of fungal partners on a single plant host can consist of dozens of individuals. However, the factors that govern competition and coexistence within these communities are still poorly understood. In this study, we used in vitro competitive assays between five ectomycorrhizal fungal strains to examine how competition and pH affect fungal growth. We also tested the ability of evolutionary history to predict outcomes of fungal competition. We found that the effects of pH and competition on fungal performance varied extensively, with changes in growth media pH sometimes reversing competitive outcomes. Furthermore, when comparing the use of phylogenetic distance and growth rate in predicting competitive outcomes, we found that both methods worked equally well. Our study further highlights the complexity of ectomycorrhizal fungal competition and the importance of considering phylogenetic distance, ecologically relevant traits, and environmental conditions in predicting the outcomes of these interactions.

Thermal traits govern the response of microbial community dynamics and ecosystem functioning to warming

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Understanding the ecological processes that underpin the dynamics of community turnover in response to environmental change is critical to predicting how warming will influence ecosystem functioning. Here, we quantify the effect of changing temperature on community composition and ecosystem functioning via the action of ecological selection on population-level thermal traits. To achieve this, we use microbes isolated from a network of geothermal streams in Iceland where in situ temperatures span 8–38°C within a single catchment. We first quantified variability in thermal tolerance between taxa, and then assembled synthetic communities along a broad thermal gradient to explore how temperature-driven selection on thermal tolerance traits shaped the emergent community structures and functions. We found marked changes in community structure and composition with temperature, such that communities exposed to extreme temperatures (10, 35°C) had highly asymmetric biomass distributions and low taxonomic richness. Thermal optima were a good predictor of the presence and relative abundance of taxa in the high-temperature treatments. We also found that the evenness of the abundance distribution was related to ecosystem production, such that communities with more equitable abundance distribution were also the most productive. Our results highlight the utility of using a multi-level approach that links population-level traits with community structure and ecosystem functioning to better understand how ecological communities will respond to global warming.

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Article

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ECOL LETT

The history of species immigration can dictate how species interact in local communities, thereby causing historical contingency in community assembly. Since immigration history is rarely known, these historical influences, or priority effects, pose a major challenge in predicting community assembly. Here, we provide a graph‐based, non‐parametric, theoretical framework for understanding the predictability of community assembly as affected by priority effects. To develop this framework, we first show that the diversity of possible priority effects increases super‐exponentially with the number of species. We then point out that, despite this diversity, the consequences of priority effects for multispecies communities can be classified into four basic types, each of which reduces community predictability: alternative stable states, alternative transient paths, compositional cycles and the lack of escapes from compositional cycles to stable states. Using a neural network, we show that this classification of priority effects enables accurate explanation of community predictability, particularly when each species immigrates repeatedly. We also demonstrate the empirical utility of our theoretical framework by applying it to two experimentally derived assembly graphs of algal and ciliate communities. Based on these analyses, we discuss how the framework proposed here can help guide experimental investigation of the predictability of history‐dependent community assembly. How predictable is the assembly of species‐rich communities? We provide a graph‐based, non‐parametric, theoretical framework for understanding the predictability of community assembly as affected by priority effects.

Ecophylogenetics redux

Article

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Feb 2021
ECOL LETT

T. Jonathan Davies

Species' evolutionary histories shape their present-day ecologies, but the integration of phylogenetic approaches in ecology has had a contentious history. The field of ecophylogenetics promised to reveal the process of community assembly from simple indices of phylogenetic pairwise distances - communities shaped by environmental filtering were composed of closely related species, whereas communities shaped by competition were composed of less closely related species. However, the mapping of ecology onto phylogeny proved to be not so straightforward, and the field remains mired in controversy. Nonetheless, ecophylogenetic methods provided important advances across ecology. For example the phylogenetic distances between species is a strong predictor of pest and pathogen sharing, and can thus inform models of species invasion, coexistence and the disease dilution/amplification effect of biodiversity. The phylogenetic structure of communities may also provide information on niche space occupancy, helping interpret patterns of facilitation, succession and ecosystem functioning - with relevance for conservation and restoration - and the dynamics among species within foodwebs and metacommunities. I suggest leveraging advances in our understanding of the process of evolution on phylogenetic trees would allow the field to progress further, while maintaining the essence of the original vision that proved so seductive.

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Article

Aug 2021

Advances in next-generation sequencing have enabled the widespread measurement of microbiome composition across systems and over the course of microbiome assembly. Despite substantial progress in understanding the deterministic drivers of community composition, the role of historical contingency remains poorly understood. The establishment of new species in a community can depend on the order and/or timing of their arrival, a phenomenon known as a priority effect. Here, we review the mechanisms of priority effects and evidence for their importance in microbial communities inhabiting a range of environments, including the mammalian gut, the plant phyllosphere and rhizosphere, soil, freshwaters and oceans. We describe approaches for the direct testing and prediction of priority effects in complex microbial communities and illustrate these with re-analysis of publicly available plant and animal microbiome datasets. Finally, we discuss the shared principles that emerge across study systems, focusing on eco-evolutionary dynamics and the importance of scale. Overall, we argue that predicting when and how current community state impacts the success of newly arriving microbial taxa is crucial for the management of microbiomes to sustain ecological function and host health. We conclude by discussing outstanding conceptual and practical challenges that are faced when measuring priority effects in microbiomes. The order and timing of the arrival (priority effects) of members of a microbiome can influence microbiome composition and function. In this Review, Debray and colleagues provide an overview of the mechanisms of priority effects, highlight examples in host-associated and environmental communities, and discuss methods to detect priority effects in microbial communities.

Functional diversity (FD), species richness, and community composition

Article

Full-text available

May 2002
ECOL LETT

Functional diversity is an important component of biodiversity, yet in comparison to taxonomic diversity, methods of quantifying functional diversity are less well developed. Here, we propose a means for quantifying functional diversity that may be particularly useful for determining how functional diversity is related to ecosystem functioning. This measure of functional diversity ''FD'' is defined as the total branch length of a functional dendrogram. Various characteristics of FD make it preferable to other measures of functional diversity, such as the number of functional groups in a community. Simulating species' trait values illustrates how the relative importance of richness and composition for FD depends on the effective dimensionality of the trait space in which species separate. Fewer dimensions increase the importance of community composition and functional redundancy. More dimensions increase the importance of species richness and decreases functional redundancy. Clumping of species in trait space increases the relative importance of community composition. Five natural communities show remarkably similar relationships between FD and species richness.

The Origin of Species

Book

Jan 1998

Charles Darwin

Functional redundancy supports biodiversity and ecosystem function in a closed and constant environment

Article

Jun 2004

The role functionally redundant species play in ecosystem function has not been adequately investigated. To study this, we examined species richness and an ecosystem function, cellulose decomposition, while environmental conditions were held constant. Our hypotheses were (1) increasing species richness will have no effect on rates of cellulose decomposition and (2) species richness will decline over time in functionally redundant communities. A relatively simple microcosm-based system to manipulate complex microbial interactions was employed. Microcosms containing cellulose as the sole carbon source were inoculated at equal densities with none, one, two, four, or eight species of cellulolytic bacteria. At 5-d intervals for 25 d, community composition and cellulose decomposition were determined. We rejected both of our hypotheses. In a constant environment, greater species richness supported a greater number of individuals and subsequently greater rates of total cellulose decomposition. Furthermore, greater initial species richness maintained greater richness over time. These results provide experimental evidence that functionally redundant species may play an integral role in ecosystem function.

Measurement of "Overlap" in Comparative Ecological Studies

Article

Sep 1966

Henry S. Horn

Objective, empirical measures of overlap between samples of items distributed proportionally into various qualitative categories are presented and reviewed. These indices of overlap, derived from either probability or information theory, should prove useful to the ecologist in comparative studies of diet, habitat preference, seasonal patterns of abundance, faunal lists, or similar data.

Community-Assembly Mechanics and the Structure of an Experimental Species Ensemble

Article

Jan 1991

James A. Drake

-It was,relatively easy to produce,alternative community,states as a function,of variability in a sequence,of species invasions,employed,to assemble,a community.,Numerous mechanisms,and processes,are capable,of producing,both temporary,and nonrecoverable,differ- ences in community structure. They include priority effects, intransitivities, emergent properties (e.g., vulnerability to invasion, specific topologies), and effects specific to differences in assem- bly sequences themselves. In ecological systems, the existence of alternative states presents a difficult comparative,problem,in the,search,for unifying,principles,that,might,underlie community-level,organization. This problem,can be solved only if we understand,the cause of alternative states and determine whether such states are persistent or transient. Otherwise,

Assembly of Species Communities

Article

Nov 1974

J. M. Diamond

Alternative stable states, trait dispersion and ecological restoration

Article

Feb 2006
OIKOS

Didham et al. suggested that abiotically structured communities showing trait under-dispersion are more likely to exhibit alternative stable states than are competitively structured communities showing trait over-dispersion. We argue that the opposite is the logical expectation, and discuss implications for ecological restoration at local and regional scales.

Phylogenies and Community Ecology

Article

Nov 2002
Annu Rev Ecol Systemat

Key Words community assembly and organization, phylogenetic conservatism, biogeography, species diversity, niche differentiation s Abstract As better phylogenetic hypotheses become available for many groups of organisms, studies in community ecology can be informed by knowledge of the evo-lutionary relationships among coexisting species. We note three primary approaches to integrating phylogenetic information into studies of community organization: 1. examining the phylogenetic structure of community assemblages, 2. exploring the phylogenetic basis of community niche structure, and 3. adding a community context to studies of trait evolution and biogeography. We recognize a common pattern of phy-logenetic conservatism in ecological character and highlight the challenges of using phylogenies of partial lineages. We also review phylogenetic approaches to three emer-gent properties of communities: species diversity, relative abundance distributions, and range sizes. Methodological advances in phylogenetic supertree construction, charac-ter reconstruction, null models for community assembly and character evolution, and metrics of community phylogenetic structure underlie the recent progress in these ar-eas. We highlight the potential for community ecologists to benefit from phylogenetic knowledge and suggest several avenues for future research.

The Unified Neutral Theory of Biodiversity and Biogeography

Chapter

Jan 2001
Monogr Popul Biol

Stephen Hubbell

Conservation evaluation and phylogenetic diversity

Article

Dec 1992
BIOL CONSERV

Daniel Faith

Protecting biological diversity with limited resources may require placing conservation priorities on different taxa. A system of priorities that reflects the value of taxonomic diversity can be achieved by setting priorities such that the subset of taxa that is protected has maximum underlying feature diversity. Such feature diversity of taxon subsets is difficult to estimate directly, but can be predicted by the cladistic/phylogenetic relationships among the taxa. In this study, a simple measure of phylogenetic diversity is defined based on cladistic information. The measure of phylogenetic diversity, PD, is contrasted with a measure of taxic diversity recently developed by Vane-Wright et al. (Biol. Conserv., 55, 1991). In re-examining reserve-selection scenarios based on a phylogeny of bumble bees (Apidae), PD produces quite different priorities for species conservation, relative to taxic diversity. The potential application of PD at levels below that of the species is then illustrated using a mtDNA phylogeny for populations of crested newts Triturus cristatus. Calculation of PD for different population subsets shows that protection of populations at either of two extremes of the geographic range of the group can significantly increase the phylogenetic diversity that is protected.