Why do placentas evolve? A test of the life-historyfacilitation hypothesis in two clades in the genusPoeciliopsis representing two independent origins ofplacentasRonald D. Bassar*,†, Sonya K. Auer† and David N. Reznick

Department of Biology, University of California, Riverside, California 92521, USA

Summary

1. Most of what we know about placentas comes from mammals, yet little can be learned from

them about the adaptive significance of the placental mode of reproduction because they all

derived their placenta from a single common ancestor that lived over 100 million years ago.

We can make inferences about the adaptive significance of placentation from fish in the family

Poeciliidae because there have been multiple, recent origins of placentation, affording an

opportunity to compare close relatives with and without placentas and to seek properties that

are common to each origin of placentation.

2. Here, we used field collections and a common garden study to quantify the degree of pla-

centation and related it to aspects of the life history in two clades of live-bearing fish from the

genus Poeciliopsis that each contains an independent origin of placentation. Doing so enables

us to test the ‘life history facilitation hypothesis’, or the proposal that the placenta evolved to

facilitate the evolution of some other feature of the life history.

3. We found that the evolution of placentation in each clade is tightly correlated with the evo-

lution of other components of the life history, but that the nature of the association is radically

different across the two clades. In the Northern Clade the magnitude of post-fertilization

maternal provisioning is negatively correlated with age at maturity, mass at maturity, offspring

dry mass and interlitter interval. In contrast, degree of matrotrophy in the Southern Clade is

positively correlated with age at maturity, mass at maturity, offspring dry mass and inter-litter

interval.

4. There is thus no consistent relationship between the evolution of placentas and other fea-

tures of the life history, which negates those proposals that the placenta evolved to facilitate

the evolution of other features of the life history. However, there is a negative correlation

between degree of placentation and ovary dry mass and reproductive allocation common to

both clades, suggesting that placentation may be an adaptation that facilitates a reduction in

reproductive allocation.

Key-words: life-history evolution, live-bearing fish, matrotrophy, placenta

Introduction

Complex adaptations, such as the vertebrate eye or the

mammalian placenta, are generally common to large

groups of organisms, all of whom inherited the character

from a single, ancient common ancestor. We typically have

no knowledge of the circumstances in which the character

evolved or any transitional states in the evolution of the

character found in living descendants. This combination of

circumstances means that we have little means for inferring

how or why complex traits evolve. Here, we present the

unusual circumstance of the evolution of placentation in

the fish family Poeciliidae. We have established that there

have been multiple independent origins of placentas within

*Correspondence author. E-mail: rdbassar@yahoo.com† Present address. Department of Environmental Conservation,

University of Massachusetts, Amherst, Massachusetts 01003,

USA.

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society

Functional Ecology 2014 doi: 10.1111/1365-2435.12233

the Poeciliidae and that there are often close relatives who

either do or do not have a placenta, plus species that vary

in the extent of placentation (Reznick, Mateos & Springer

2002; Pires, Arendt & Reznick 2010; Meredith et al. 2011).

Such circumstances enable us to test hypotheses for why

placentas evolved and in other ways make inferences about

the adaptive significance of placentation that would never

be possible for mammals because they lack the necessary

variation.

A broad diversity of reproductive modes, ranging from

internal versus external fertilization or oviparity versus

viviparity, is found throughout the natural world. The evo-

lution of viviparity requires the prior evolution of internal

fertilization. Within viviparous organisms, strategies for

providing nourishment to developing offspring fall along a

continuum that ranges from lecithotrophy, wherein all

nourishment for growth and development of offspring is

provided prior to fertilization, to matrotrophy, wherein

offspring are provided with nourishment throughout their

development (Wourms, Grove & Lombardi 1988;

Blackburn 2000). The most well-known example of matro-

trophic organisms are the placental mammals, whose post-

fertilization provisioning of offspring is facilitated by a

placenta, defined as an integration of maternal and embry-

onic tissues that are specialized for the physiological main-

tenance of the developing young (Mossman 1937). To

these criteria, we add that the placenta must also be

adapted for the transfer of nutrients from the mother to

developing young. Matrotrophy as a generalized strategy

is not restricted to placental mammals. It has evolved inde-

pendently numerous times across a wide spectrum of

organisms, including terrestrial and aquatic gastropods

(Baur 1994; Von Rintelen & Glaubrecht 2005), clams

(Korniushin & Glaubrecht 2003), pseudoscorpions (Mak-

ioka 1968), flies (Meier, Kotrba & Ferrar 1999), cock-

roaches (Williford, Stay & Bhattacharya 2004), isopods

(Warburg & Rosenberg 1996), elasmobranchs (Hamlett &

Hysell 1998), several groups of bony fish (Wourms, Grove

& Lombardi 1988; Reznick, Mateos & Springer 2002),

amphibians (Wake 1993; Greven 1998) and reptiles (Stew-

art 1992). Across these taxa, matrotrophy is characterized

by a spectrum of complex morphological structures and

physiological pathways. Some matrotrophic species have

evolved the functional equivalent of the mammalian

placenta.

Virtually, all hypotheses proposed for the evolution of

matrotrophy are independent of the framework of life-his-

tory theory, one exception being the model proposed by

Trexler & DeAngelis (2003). Most of these hypotheses are

ad hoc in the sense that they are ideas suggested by the

study of life histories of one or a few matrotrophic species.

Many of them suggest that matrotrophy evolved to facili-

tate the evolution of some other feature of the life history.

For example, it has been proposed that matrotrophy

evolved to facilitate the evolution of larger litter size, lar-

ger offspring size at birth, improved survivorship early in

life or earlier maturity (Thibault & Schultz 1978;

Blackburn, Vitt & Beuchat 1984; Wourms & Lombardi

1992; Wourms 1993; Trexler 1997; Holbrook & Schal

2004; Schrader & Travis 2005; Wildman et al. 2006). We

reference these hypotheses collectively as ‘life history facili-

tation hypotheses’ because they all share the attribute of

predicting that matrotrophy evolves to facilitate the evolu-

tion of some other life-history trait.

Pires et al. (2011) tested the life-history facilitation

hypothesis in six species from the Northern Clade of the

fish genus Poeciliopsis. Three of these fish species lack

matrotrophy and three have matrotrophy that varies from

sustaining a 10% increase (P. occidentalis) to an eightfold

increase (P. prolifica) in the dry mass of the developing

young between fertilization and birth. A general way of

evaluating the plausibility of the life-history facilitation

hypothesis is to ask whether this graded increase in post-

fertilization provisioning is predictably associated with the

evolution of other components of the life history. Pires

et al. (2011) found that the evolution of matrotrophy was

tightly correlated with the evolution of earlier maturity, a

smaller size at maturity, an increase in the rate of produc-

tion of offspring early in life and the production of smaller

offspring. These trends support those life-history facilita-

tion hypotheses that suggest that the evolution of the pla-

centa facilitates the evolution of earlier maturity and an

increase in the rate of offspring production.

Pires et al. (2011) results also suggest a possible bridge

between the evolution of matrotrophy and the more gen-

eral demographic theory of life-history evolution. The con-

stellation of life-history attributes associated with the

evolution of matrotrophy in the Northern Clade of Poecili-

opsis is the same that is predicted to evolve in response to

exposure to high extrinsic rates of adult mortality or to

high mortality rates across all age classes (Roff 1992;

Stearns 1992). If the evolution of matrotrophy is indeed

consistently associated with this same complex of life-his-

tory traits and if it is also associated with species that

experience high extrinsic mortality rates, then we can

incorporate the evolution of matrotrophy into this more

general life-history framework.

A virtue of the genus Poeciliopsis is that it contains

three independent origins of extensive matrotrophy (Rez-

nick, Mateos & Springer 2002). The Southern Clade of

this genus consists of six described species, four of which

are lecithotrophic and two of which have extensive matro-

trophy, sufficient to sustain a greater than a 30-fold

increase in the dry mass of offspring between fertilization

and birth (Reznick, Mateos & Springer 2002). Here, we

take the next step in evaluating the generality of Pires

and colleagues’ results by repeating their study on the

Southern Clade and comparing associations between

matrotrophy and the life history among the two clades,

each representing an independent origin of matrotrophy.

If their results are general, then we should obtain the

same associations between the evolution of matrotrophy

and the evolution of the rest of the life history as seen in

the Northern Clade.

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology

2 R. D. Bassar et al.

Materials and methods

The genus Poeciliopsis (Cyprinodontiformes: Poeciliidae) contains

20 described viviparous species that inhabit Pacific slope drainages

from southern Arizona, USA, to Colombia (Mateos, Sanjur &

Vrijenhoek 2002). All species in Poeciliopsis have the ability to

carry multiple, simultaneous litters (superfetation). The number of

simultaneous litters varies from two to five across the genus

(Turner 1937, 1947; Scrimshaw 1944; Thibault & Schultz 1978). In

the placental species, resources are transferred from the mother to

the developing offspring via the follicular placenta (Turner 1939,

1940, 1947; Grove & Wourms 1991, 1994; Wourms & Lombardi

1992), which is an integration of maternal tissue (the follicle) with

either a modified yolk sac or externalized pericardial membrane of

the embryo. Reznick, Mateos & Springer (2002) present descrip-

tions of the pattern of maternal provisioning for all but one spe-

cies in the genus and combine them with the phylogeny to make

inferences about the evolution of maternal provisioning in this

genus. They demonstrate that provisioning across species can

range from having virtually no post-fertilization provisioning to

having nearly a 120-fold increase in the dry mass of offspring

between fertilization and birth. They also established that there

have been three independent origins of placentation within the

genus.

STUDY SPEC IES AND COLLECT ION S ITES

In the first portion of this paper, we quantify the association

between the degree of matrotrophy and the life history in species

of the Southern Clade of Poeciliopsis. The Southern Clade is fur-

ther subdivided into two clades, the first containing P. fasciata,

P. latidens and P. baenschi and the second containing P. catema-

co, P. hnilicki, P. gracilis, P. turneri, P. presidionis, P. scarlii and

P. turrubarensis (Mateos, Sanjur & Vrijenhoek (2002). The South-

ern Clade contains only one independent origin of matrotrophy,

in the common ancestor of P. presidionis and P. turneri (Reznick,

Mateos & Springer 2002), so we only considered the seven species

from the second clade in the current study.

We examined the association between matrotrophy and the life

history in the wild and laboratory using field collections and a

common garden experiment on the second generation of labora-

tory born offspring from wild-caught parents, respectively. Fish

from the field collections of all seven species and 16 localities (up

to four populations per species) were either collected by ourselves

or were subsets of collections from museums (Appendix S1, Sup-

porting information). We included only 4 of these species (the leci-

thotrophic species P. gracilis, P. scarllii, and the matrotrophic

species P. turneri and P. presidionis) in the laboratory common

garden analysis. P. scarllii was represented by two populations

(Rio Tomatlan and Rio San Blas). Founders for our laboratory

stocks for these populations were collected by D. Reznick, M.

Pires and M. Mateos in May 2003 and January 2004 (Appendix

S1, Supporting information).

In the second portion of this paper, we present combined analy-

ses of the Northern and Southern Clades. To do so, we include

data from the Northern Clade originally presented by Pires et al.

(2011). Details of the collection sites for the Northern Clade can

be found in Pires et al. (2011).

DISSECT ION OF F IELD COLLECTED F ISH

We quantified the life histories of each collection – including the

minimum and mean size of reproducing females, number of off-

spring per litter, degree of superfetation, ovary dry mass, mean

offspring mass and reproductive allocation – and the degree of

matrotrophy using similar protocols as done for the Northern

Clade (Pires et al. 2011) to facilitate comparison. We determined

female size by measuring standard length and weighing individual

somatic dry mass. Developing offspring and associated reproduc-

tive tissues were removed from each female, litters were separated

based on stage of development and the number of litters and num-

ber of offspring in each litter were quantified (Reznick 1981, 1982;

Haynes 1995; Pires et al. 2011). Litter size was defined as the num-

ber of offspring in a litter of offspring of similar developmental

stage. The degree of superfetation was measured as the number of

distinct litters a female was carrying at the time of dissection.

Ovary dry mass was determined by drying and then weighing

developing offspring and reproductive tissues. Mean offspring

mass was calculated as the dry mass of all individual offspring in a

litter divided by the number of offspring in the litter. Reproductive

allocation (RA) was defined as the percentage of total dry mass of

the females that was devoted to reproduction at the time of dissec-

tion and was calculated as the ovary dry mass divided by the total

dry mass of the female.

We then estimated the degree of matrotrophy using the Matro-

trophy Index (MI) for each individual. MI is the average dry mass

at birth divided by the average dry mass of eggs with blastodiscs

(Reznick, Mateos & Springer 2002) and is similar to other

approaches used in other taxa (Wourms, Grove & Lombardi

1988; Stewart & Thompson 2003; Thompson & Speake 2006). If a

female fully provisions eggs prior to fertilization, then MI has a

value <1, usually in the vicinity of 0�6–0�7, because the embryos

lose mass between the time when the egg is fertilized and when the

embryo is born. If there is substantial post-fertilization provision-

ing, MI is instead >1. For example, P. prolifica from the Northern

Clade has MI values in the vicinity of eight, which means that

there is, on average, an eightfold increase in dry mass between

fertilization and birth (Pires, McBride & Reznick 2007).

LABORATORY STUDIES

We then examined covariation among matrotrophy and the life-

history traits through common garden laboratory experiments,

using protocols similar to those as used for the Northern Clade

(Pires et al. 2011) to facilitate comparison. The virtue of the labo-

ratory studies is that they enable us to control for environmental

effects and to quantify additional life-history variables. Briefly,

wild-caught fish were brought to the laboratory and raised to at

least the second generation in a common lab environment to

reduce variation among species that might arise from maternal

and environmental effects. Siblings were placed together in groups

of five individuals in 8 L aquaria on the day they were born and

were fed a diet of liver paste in the morning and brine shrimp nau-

plii in the afternoon on a daily basis until they reached a weight

of 30 micrograms. As offspring number and size at birth vary

between species, the time interval between birth and placement in

the experiments differed between species. For the Southern Clade

species, P. presidionis and P. turneri reached the designated mass

within 5–8 days of age, while it took approximately 25 days for

P. gracilis and P. scarlii populations to attain that mass.

Once they reached 30 mg, fish were placed in the experiment

under one of two separate experimental designs. In design 1, indi-

vidual F2 fish were placed in separate 8 L aquaria and positioned

in the laboratory based on a randomized block design wherein

each block contained four tanks of each species, but the orders of

the species or population group on the shelves were randomly

assigned across blocks. All species in a block were set up within

1 week of each other to keep setup time relatively constant. Once

their male siblings or cohort members began to show signs of

reaching maturation, mature stock tank males were added to the

female tanks for 1 week, every other week, to serve as mates. We

timed the addition of males this way because prior research

(Reznick 1982) revealed that males and females mature at

approximately the same rate, so the maturation of brothers can

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology

Matrotrophy and life history 3

serve as an indicator of the approaching maturity of their sisters.

Providing mature males shortly before females attain maturity

assures that females will mate as soon as they are capable of

reproducing.

Some species did not reliably produce offspring under design 1,

so we also employed a modification of this design, hereafter design

2. After individuals obtained the appropriate size for placement in

the study and before their age at first parturition, they were placed

in species-specific 20 L group tanks instead of individual 8 L

tanks as done in design 1. Six individuals per species per block

were housed in each of these group tanks. Once the experimental

fish were large enough to avoid risk of being cannibalized, two

mature stock tank males were added to the tanks as mates. Devel-

oping males were moved to 8 L aquaria when their gonopodium

began to elongate. All females were removed once offspring

appeared in the group tank (i.e. when the first female had given

birth). Once individuals were removed, they were placed in the

randomized block setup described for design 1.

As done by Pires et al. (2011) and in prior common garden

studies (e.g. Reznick & Bryga 1996), we reared fish at two different

ration levels for design 1. Within each species or population of a

block, fish were randomly assigned to either a high or low food

ration. High and low food rations were identical across species

and populations. In design 2, all fish were fed ad libitum food for

the duration of the experiment.

In both designs, tanks were checked daily to determine the sex

of the individuals and to check for newly born offspring in female

only and group tanks. The maturation status of males was

checked by observing the degree of metamorphosis in the anal fin,

and males were considered mature when the barbed tip of the go-

nopodium was no longer covered by protective cells (Turner

1941). Once mature, males were euthanized using an overdose of

MS-222 and their standard length and wet mass were measured.

When new offspring were observed in female tanks, the offspring

were removed, enumerated, euthanized using an overdose of MS-

222, and preserved in 5% formalin for later determination of dry

mass. Females were euthanized and preserved in 5% formalin

60 days after first parturition. Sixty days is approximately two

times the amount of time required for an embryo to develop from

fertilization to birth. This time interval was thus sufficient for us

to collect four or more litters of young from these species because

they all have superfetation. All experiments were conducted in the

vivarium at the University of California, Riverside (UCR) under

protocols approved by the UCR Institutional Animal Care and

Use Committee.

We measured MI and the same life-history traits as in Pires

et al. (2011), including age and wet mass at first parturition, num-

ber of offspring per litter, degree of superfetation, ovary dry mass,

mean offspring mass, reproductive allocation, and interlitter inter-

val. Number of offspring per litter, degree of superfetation, ovary

dry mass, mean offspring mass, reproductive allocation and the

degree of matrotrophy were measured using the same protocols as

described previously for the field collections. We used age and

mass at first parturition as a proxy for maturity because females

in this genus have no external clues to mark the time of their

maturity. Interlitter interval was defined as the duration, in days,

between the births of two consecutive litters.

STAT IST ICAL ANALYSES

We first examined whether there were significant differences in the

suite of life-history traits among species and populations in the

laboratory stocks using multivariate analyses of variance (MANO-

VA). We included age and wet mass at first parturition, offspring

size, litter size, degree of superfetation, interlitter interval and

ovary dry mass as variables that describe the life history. We

excluded the MI from this analysis because our ultimate goal was

to see whether MI predicts the patterns of life-history variation.

We also excluded ova dry mass and RA from the multivariate

analyses. Ova dry mass is in the denominator of the ratio used to

estimate MI and RA is derived from female wet mass, so these

two traits were known a priori to be correlated with MI and

female wet mass at first parturition, respectively. Ovary dry mass,

which is the mass of all developing embryos and associated repro-

ductive tissue, was used instead of RA in multivariate analyses.

We then employed discriminant function analysis (DFA) to

characterize the contributions of individual dependent variables to

the differences among species. We evaluated canonical variables

from the DFA with eigenvalues greater than one (first three) to

determine which of the canonical variables was primarily responsi-

ble for the separation among species. We used the probability of

correct classification as a measure of the degree of separation

among species. Next, we used bivariate correlation analyses to

determine whether any of the canonical variables was correlated

to MI. Finally, we examined the total canonical structure of any

canonical axis that was related to MI to determine which of the

life-history traits was mostly associated with that axis and ulti-

mately the degree of matrotrophy. The total canonical structure is

equivalent to the bivariate correlation between the score on the

canonical variable and the life-history traits used to construct it.

Individual level data were used for this analysis.

We utilized a similar approach for the life-history analysis of

fish from the wild collections. However, instead of DFA, we per-

formed a principle components analysis (PCA) on the population

means of each life-history trait. We took this approach because

using individual level data in a DFA would force us to reduce the

number of life-history traits we could examine in this collection.

So, using the PCA allowed us to examine the multivariate rela-

tionship among life-history traits, but did not allow us to explicitly

test for differences among populations in the life histories. We

used a modified suite of variables for the PCA because the vari-

ables estimated from the field samples were not identical to those

estimated in the laboratory. The life-history traits for the field

analyses included minimum size of reproductive females (a field

surrogate for the size at first parturition), the mean level of super-

fetation, the mean number of offspring per litter, the projected

mass of offspring at birth (derived from a regression that describes

the relationship between stage of development and offspring mass)

and the mean total reproductive mass (the dry mass of all develop-

ing embryos and ovarian tissues). We retained the first three prin-

ciple components and calculated the factor loadings (bivariate

correlations between each principle component and the life-history

traits). Similar to the DFA for the laboratory populations, we

then used bivariate correlations to test for significant correlations

between each principle component axis and the degree of matro-

trophy. The multivariate analyses of the field and laboratory data

were conducted in a conventional, non-phylogenetic fashion (i.e.

assuming a star phylogeny). We also tested separately for relation-

ships between matrotrophy and each life-history character in the

laboratory and field populations of the Southern Clade using

bivariate correlations, but results were qualitatively similar to

those from the multivariate analyses (Appendix S2, Supporting

information).

Finally, we tested for differences between the two clades in their

relationship between matrotrophy and each life-history character.

We started by including the same life-history traits in both clades

as dependent variables in a multivariate analysis of variance (MA-

NOVA). Independent predictors included clade entered as fixed

effect, natural log transformed MI as a covariate and the interac-

tion between clade and MI. A significant interaction between clade

and MI would mean that the multivariate relationship between

the life-history variables and MI differed among the independent

origins of matrotrophy. Individual level data from only the lab

study were used in this analysis. Next, we used a regression

approach to analysis of covariance (ANCOVA) to evaluate which

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology

4 R. D. Bassar et al.

traits contributed to similarities and differences in the relationship

between MI and the life-history traits between the clades. The

value of the life-history trait was included as the dependent vari-

able and MI was included as a covariate. Clade was entered as a

fixed effect and was dummy coded as 0 or 1. The interaction

between clade and MI was included to test for differences in the

relationship between the life-history trait and matrotrophy

between the two clades, but interactions were subsequently

removed if non-significant (P > 0�05).Analyses of the bivariate relationships in the Southern Clade

alone and univariate comparisons of these relationships between

the two clades were conducted on population means using both

raw data (i.e. ‘star phylogeny’) and data corrected for phyloge-

netic relationships using phylogenetic generalized least-squares

(PGLS). These analyses were conducted using the Matlab pro-

gram REGRESSION.m (Ives, Midford & Garland 2007). We

employed the most current evolutionary hypothesis for the phylo-

genetic relationship among the Poeciliopsis species (Mateos, San-

jur & Vrijenhoek 2002) and used arbitrary branch lengths because

the divergence time between species or populations was unknown

(Pagel 1992). For both the laboratory and field collections, popu-

lations within species were included as soft polytomies with

branch lengths set to 0�5. We compared the likelihoods of both

the star and PGLS analyses to determine which provided a better

fit to the data.

Results

SOUTHERN CLADE

Laboratory-reared populations: The MANOVA showed that

a significant amount of the variation in life-history traits

were attributable to differences among species (Wilks’

k28,192�5 = 0�003, P < 0�0001, Fig. 1). The subsequent DFA

showed that all individuals were correctly classified to spe-

cies. The only misclassifications were between the two pop-

ulations of P. scarlii. In total, two of ten individuals

(20%) from Rio San Blas were misclassified as being from

the Rio Tomatlan population. The first canonical variable

accounted for 88% of the variation in the life-history traits

among the species and was positively correlated with MI

(r = 0�99, d.f. = 3, P < 0�001, Table 1, Fig. 2). This signifi-

cant correlation shows that the evolution of increased MI

in this clade is indeed correlated with the evolution of a

complex of other life-history traits. Specifically, the evolu-

tion of increased MI is correlated with the evolution of

delayed age at maturity, a larger body size at maturity, a

higher degree of superfetation, reduced litter size, reduced

ovary dry mass, but increased offspring size at birth

(Table 1). Of all the life-history traits, only interlitter inter-

val showed no relationship with the first canonical vari-

able. The other axes accounted for much less variation and

were not significantly related to the degree of matrotrophy

(Table 1).

Field collected populations: The PCA yielded two prin-

ciple components which accounted for similar propor-

tions of the total variation (PC1 = 42�9% and

PC2 = 35�6%; Table 1B). PC1 was not significantly cor-

related with MI, but PC2 was (Table 1B, Fig. 2d–f). The

qualitative weighting of the dependent variables in PC2

was the same as in the analysis of the laboratory data.

Increased MI was associated with a decrease in the num-

ber of offspring per litter but an increase in the minimum

size of reproducing females (a surrogate estimate of the

size at maturity), degree of superfetation, offspring size

and ovary dry mass.

COMPARISONS WITH THE NORTHERN CLADE

Laboratory-reared populations: The multivariate analysis

(MANOVA) that included age at maturity, mass at maturity,

offspring size, offspring number, level of superfetation, in-

terlitter interval and ovary dry mass as dependent variables

showed that the relationship between these life-history

traits and MI was significantly different among the clades

(Clade x MI: Wilks’ k7,125 = 0�115, P < 0�0001). In the uni-

variate analyses, for all life-history traits, analyses based

on star-phylogenies yielded higher log-likelihoods com-

pared to the analyses that included phylogenetic correc-

tions (Table 2). The two clades were similar to each other

in the relationship between MI and the number of off-

spring per litter, reproductive allocation and ovary dry

mass. In both clades and in both the laboratory and field

collections, increased MI was related to giving birth to

fewer offspring per litter, smaller ovary dry masses and

lower values for reproductive allocation (Table 2, Fig. 3).

There were significant interactions among clades for the

relationship between MI and all other dependent variables.

The interaction between MI and offspring size was the

most dramatic. In the Northern Clade, matrotrophic spe-

cies gave birth to smaller babies relative to lecithotrophic

(a)

(b)

Fig. 1. Ordinations of the five populations used in the laboratory

study on canonical variables 1 and 2 (a) and canonical variables 3

and 4 (b). Small symbols represent the scores for the individual fish

and the large symbols represent the centroids for each population.

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology

Matrotrophy and life history 5

species, while in the Southern Clade, matrotrophic species

instead gave birth to larger babies relative to more lecitho-

trophic species (Table 2, Fig. 3). The interactions for the

remaining variables also revealed significant, but less

marked differences among clades in how life histories

change in association with the evolution of placentation.

In the Northern Clade, increased matrotrophy was associ-

ated with a significant decline in the age and size at matu-

rity. In the Southern Clade, increased MI was instead

associated with a trend, not significant, towards larger size

and later age at maturation (Table 2, Fig. 3, and Appen-

dix S2, Supporting information). Likewise, the evolution

of increased MI was associated with significantly shorter

interlitter intervals in the Northern Clade, but with a non-

significant trend towards longer intervals in the Southern

Clade (Table 2, Fig. 3, and Appendix S2, Supporting

information). Increased MI was related to higher degrees

of superfetation in both clades. In the Northern Clade,

there was a significant increase in superfetation in associa-

tion with increased MI, while in the Southern Clade there

was a non-significant positive correlation between MI and

superfetation (Table 2, Fig. 3, and Appendix S2, Support-

ing information). Finally, both clades showed a negative

relationship between MI and ova dry mass, but the rela-

tionship was steeper in the Northern Clade (Table 2,

Fig. 3). The preponderance of significant interactions

between MI and clade for so many dependent variables is

a signature of the differences between the clades in the

association between the evolution of MI and the evolution

of the remainder of the life history.

Field collected populations: Patterns observed for the

field collected populations were the same as those

described earlier for the laboratory-reared populations.

Again, analyses based on star-phylogenies yielded higher

log-likelihoods compared to the analyses that included

phylogenetic corrections (Table 2). Litter size decreased

with increasing MI in both clades and did not differ

between clades (Table 2, Fig. 4). Reproductive allocation

also decreased significantly with increase in MI in both

clades, but the Northern Clade had significantly higher

RA for a given level of matrotrophy (Table 2, Fig. 4).

There was a significant interaction between MI and clade

for the remaining life-history traits. First, increase in

matrotrophy was associated with smaller offspring in the

Northern Clade but larger offspring in the Southern Clade

(a) (d)

(b) (e)

(f)(c)

Fig. 2. Relationships between Matrotrophy Index and the first

three canonical variables (a–c) for the laboratory data and the first

three principle components for the wild collection (d–f). Canonicalvariable scores are the centroids for each species from the discri-

minant function analysis.

Table 1. Bivariate correlation coefficients between either the

canonical variables (laboratory) or the principle components

(field) and each the life-history traits. Eigenvalues and summary

statistics of the correlation between each canonical variable or

principle component and degree of matrotrophy

Canonical variable

Variable 1 2 3

(A) Laboratory data

Age at first parturition 0�341 �0�527 �0�005Female wet mass at first

parturition

0�447 �0�591 �0�361

Offspring dry mass 0�991 �0�059 0�012Litter size �0�678 0�067 0�006Superfetation 0�356 �0�533 0�184Interlitter interval �0�048 0�813 �0�377Ovary dry mass �0�867 �0�076 0�229Eigenvalues 29�3 2�5 1�2Proportion of total variance

explained

0�877 0�075 0�037

Correlation with MI 0�999 0�259 �0�114d.f. 3 3 3

P <0�001 0�674 0�855

Principle component

Variable 1 2 3

(B) Field data

Smallest size of reproductive

females

0�584 �0�075 0�525

Superfetation 0�430 �0�297 �0�812Litter size 0�284 0�641 �0�061Estimated offspring size at birth 0�412 �0�542 0�235Ovary dry mass 0�473 0�449 �0�078Eigenvalues 2�143 1�780 0�650Proportion of total variance

explained

0�429 0�356 0�130

Correlation with MI 0�340 �0�672 �0�240d.f. 14 14 14

P 0�198 0�004 0�371

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology

6 R. D. Bassar et al.

Table

2.Log-likelihoodsandtstatisticsfrom

linearmodel

withMIandcladeasindependentvariables.Analysesare

those

withastarphylogeny(‘Star’)analysedwithleast-squaresandthose

with

phylogeniccorrection(PGLS).Log-likelihoodsfrom

fullmodels(includinginteractionterm

s)werecomparedto

determinewhether

thestarphylogenyorthephylogeneticcorrectionbestfitthedata.

Inallcases,log-likelihoodsforstarphylogenyprovided

abetterfit.Non-significantinteractionswereremoved

inthesemodels,butthelog-likelihoodsfrom

thefullmodel

are

shownforcomparison

withPGLSanalyses.Degrees

offreedom

forlaboratory

studiesare

6andforwild-caughtpopulationsare

28.Allvariableswerenaturallog–transform

edpriorto

analysis.Values

inbold

are

signifi-

cantatthe0�05

level

Trait

Lab-Star

Lab-PGLS

Field-Star

Field-PGLS

Log-

likelihood

Clade

MI

Cladex

MI

Log-

likelihood

Clade

MI

Cladex

MI

Log-

likelihood

Clade

MI

Cladex

MI

Log-

likelihood

Clade

MI

Cladex

MI

Ageatfirstparturition

11

2�9

0�7

3�6

7�3

1�1

0�4

2�6

––

––

––

––

Smallestsize

*/Sizeatmaturity

†1�8

5�9

1�4

2�3

�0�4

2�5

11�8

10�6

3�9

2�7

2�9

4�3

0�8

1�1

0�9

Averagesize

ofpregnantfemales

––

––

––

––

18�2

6�0

2�4

2�6

13�4

1�2

2�1

1�7

Superfetation

�0�1

1�7

1�5

2�8

�4�2

0�6

0�9

2�7

�30�5

8�2

5�2

�15�8

0�1

2�9

1�7

Littersize

5�2

1�6

5�1

–0�6

0�7

3�9

1�5

�26�9

0�7

2�1

–�3

5�8

0�1

1�5

0�7

Offspringdry

mass

11�2

9�6

15�9

14�1

7�0

3�3

9�8

9�3

�17�4

3�4

1�2

3�2

�18�1

0�7

1�1

2

Ovary

dry

mass

�0�1

3�3

7�1

–�1

�71�4

4�5

0�1

�32

3�2

3�3

2�3

�39�8

0�6

2�1

1�3

Interlitterinterval

5�1

11�4

3�3

1�4

0�2

0�8

2�1

––

––

––

––

Ovadry

mass

10

7�5

17�2

13

5�8

2�6

10�3

8�3

––

––

––

––

Reproductiveallocation

�3�7

2�3

5�1

–�8

0�8

3�1

0�8

�19�8

2�6

3–

�28�2

0�5

0�9

0�3

Dry

weightofreproductivetissue=averagedry

weightofalleggsandem

bryosfoundin

reproductivefemales;ReproductiveAllocation=[dry

mass

ofem

bryos/(dry

mass

ofem

bryos+dry

mass

of

female)],from

fieldcollectionspreserved

inform

alinor[dry

mass

ofem

bryos/wet

mass

ofalcohol-preserved

females)*3�59

2,forfemalespreserved

inalcohol.;Estim

ateddry

weightofoffspringat

birth

=estimateddry

weightatstage45basedonparametersofregressionmodelbetweenstageofdevelopmentandem

bryonicdry

weight/litter

size

=litter

size

oftheaverage-sizedfemale(theaver-

agenumber

ofyoungper

litter,estimatedfrom

applyingtheregressionoflitter

size

onfemale

size

totheaveragefemale

length);Superfetation=averagenumber

oflittersper

female

atthetimeof

dissection;Maxim

um

number

oflittersper

female

=maxim

um

number

oflittersfoundin

afemale.

*fielddata.

†laboratory

data.

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology

Matrotrophy and life history 7

(Table 2, Fig. 4). Secondly, increased matrotrophy was

associated with a smaller minimum and mean size at matu-

ration in the Northern Clade, whereas in the Southern

Clade, increased matrotrophy was associated with a larger

minimum and mean size at maturation (Table 2, Fig. 4).

Thirdly, increasing matrotrophy was associated with a

higher degree of superfetation in both clades, but the rate

of increase was higher for the Northern Clade (Table 2,

Fig. 4). Finally, ovary dry mass significantly decreased

with increase in MI in both clades, but did so at a higher

rate in the Northern Clade (Table 2, Fig. 4).

Discussion

There was a significant association between the evolution

of MI and the evolution of the remainder of the life

history in the Southern Clade. This pattern was much

more evident in the laboratory than the field data, we

Fig. 4. Relationships between Matrotrophy

Index and each life-history trait for the

field populations. ▲/dashed line = South-

ern Clade; ●/solid line = Northern Clade.

Fig. 3. Relationships between Matrotrophy

Index and each life-history trait for the lab-

oratory-reared populations. ▲/dashed line

= Southern Clade; ●/solid line = Northern

Clade.

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology

8 R. D. Bassar et al.

presume because in the laboratory we are able to control

for environmental effects and hence reduce residual vari-

ance. We are also able to estimate a wider spectrum of life-

history variables in the laboratory, including age and size

at maturity and frequency of reproduction. These addi-

tional variables contributed to our ability to discriminate

among species that differ in maternal provisioning. The

virtue of reporting laboratory and field results is that they

enable us to generalize our observations to all species in

the clade and a larger number of populations. The correla-

tion we observed between the evolution of the maternal

provisioning and the remainder of the life history suggests

a causal relationship, as postulated by the various life-his-

tory facilitation hypotheses. The catch is that the nature of

these correlations is quite different from those in the

Northern Clade.

HOW ARE THE TWO CLADES D IFFERENT?

In the laboratory, the association between the degree of

matrotrophy and a multivariate measure of the life history

was different between the two clades. In one dependent

variable (offspring size), the relationship between the life

history and MI was the opposite in the two clades and sig-

nificant in each of them. In four dependent variables (age

at maturity, mass at maturity, superfetation and interlitter

interval), the relationship between the dependent variable

and MI was the opposite in the two clades, but the within

clade relationship was significant in only one of the clades.

In one dependent variable (ova dry mass), there was a sig-

nificant interaction between the life history and MI, but

the slopes among the clades had the same sign. Finally,

three of the nine traits (litter size, reproductive allocation

and ovary dry mass) showed no significant interaction

between the life history and MI. The different associations

between MI and age at maturity, size at maturity, off-

spring size and interlitter interval are enough to invalidate

the life-history facilitation hypotheses for Poeciliopsis.

Given such differences among such closely related clades,

we feel safe in saying that these hypotheses have no gen-

eral explanatory value and can be rejected. This also

means that there is no simple bridge to be found between

the evolution of matrotrophy and demographic life-history

theory.

We note that the same divide was revealed in a com-

parison of the life histories of fish in the family Zenar-

copteridae [fresh water half beaks; (Reznick, Meredith &

Collette 2007)]. The two genera in this study, Dermogenys

and Nomorhamphus, included species that varied in the

presence and absence of matrotrophy and superfetation;

there was at least one independent origin of matrotrophy

in each of these genera. In Dermogenys, the evolution of

increased matrotrophy was associated with the produc-

tion of fewer, larger offspring per litter. In Nomorham-

phus, the evolution of increased matrotrophy was instead

correlated with the production of more, smaller offspring

per litter.

It might be tempting to postulate that the placenta could

be adaptive in a conditional or context-specific way, such

as to enhance the evolution of offspring size in one context

but facilitate the evolution of earlier maturity and an

increased rate of offspring production early in life in

another context. However, invoking such an alternative

negates our goal of seeking a general explanation for the

evolution of the placenta. More to the point, our prior

experience in the study of life-history evolution in guppies

(Reznick, Bryga & Endler 1990; Reznick & Bryga 1996;

Reznick, Rodd & Cardenas 1996; Reznick et al. 1997)

shows that all of these life-history traits can be substan-

tially different among populations within a species and

that populations have sufficient genetic variation to sustain

rapid evolution of all of these traits, without any recourse

to their evolution being driven by the correlated evolution

of some other complex trait. Said differently, there is no

need for anything like a facilitation hypothesis to explain

the scope of life-history evolution that is displayed by this

family of fishes.

HOW ARE THESE CLADES THE SAME?

There was, however, one feature of the life history that

evolved in a consistent fashion in concert with the evolu-

tion of increased matrotrophy. In both the Northern and

Southern Clades, we found that the evolution of increased

MI was correlated with the evolution of a smaller ovary

dry mass and a lower value for reproductive allocation.

Both of these variables characterize the mass of reproduc-

tive tissues relative to somatic tissues, and presumably the

volume of developing young. The reason we see this com-

mon feature in both clades is that the evolution of

increased post-fertilization maternal provisioning is

attained primarily by reducing the size of the egg at fertil-

ization, rather than increasing the size of the offspring at

birth. When this change is combined with superfetation, it

means that early stage embryos have a much smaller mass

and volume than late stage embryos. Their combined vol-

ume, and relative dry mass, can be consistently smaller

than in non-placental species, even if there is no reduction

in the rate of offspring production. Reznick, Meredith &

Collette (2007) obtained the same result for the two inde-

pendent origins of matrotrophy in the two genera of fresh-

water halfbeaks. In spite of the differences between the

genera in the way offspring size and offspring number

change with increased MI, both lineages display a consis-

tent and significant decline in reproductive allocation in

correlation with the evolution of increased matrotrophy.

This similar trend in four out of four lineages suggests

that there could be a common adaptive explanation for the

evolution of matrotrophy in all four of them. Trexler &

DeAngelis (2003), Thibault & Schultz (1978) and Miller

(1975) proposed that placentation could be an adaptation

that reduces the profile of pregnant females and hence

reduces the cost of locomotion. It could thus serve as an

adaptation to life in streams with high flow rates.

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology

Matrotrophy and life history 9

Plaut (2002) and Ghalambor, Reznick & Walker

(2004) have shown that a locomotor cost of reproduction

exists in related lecithotrophic species of Poeciliidae,

Gambusia and Poecilia, respectively. Both of these species

lack superfetation. In their case, the cost of locomotion

increased as the single litter of young progressed through

development because, even though they were declining in

dry mass, they increased in wet mass and volume by a

factor of three to four between when the egg was fertil-

ized and when the embryo was fully developed and

ready to be born. It was this increase in wet mass and

volume that was associated with a decline in acceleration

and maximum swimming speed. Unfortunately, there

currently is no empirical data on how matrotrophic

reproduction alleviates these locomotor costs. One possi-

ble catch in applying this logic for how the evolution of

increased MI might affect ovary volume and locomotion

is that our conclusion is based on dry mass, which

implicitly assumes that it would carry over to wet mass

and volume. If species with high matrotrophy for some

reason have more moisture associated with reproductive

tissues than do lecithotrophic species, then this hypothe-

sis might not be viable.

CONFL ICT VERSUS ADAPTAT ION?

Here and in earlier publications, we have addressed most

of the proposals for the adaptive significance of placenta-

tion. All features of adaptive facilitation hypotheses, save

the possible link to ovary volume and locomotion, have

been shown to lack generality. We have also addressed

Trexler & DeAngelis’ (2003) general model for the evolu-

tion of matrotrophy and can at least show that the condi-

tions that favour the evolution of matrotrophy in the

context of their model are limited. We did so by testing

their assumption that placental species have the capacity

to fertilize a large number of small eggs with a minimum

of resources and then adjust brood size to food availability

by aborting some embryos. If they can do so, then the con-

ditions that favour the evolution of matrotrophy are far

easier to satisfy than if they cannot. We have shown in

species that represent four independent origins of placenta-

tion that placental species cannot abort embryos in

response to low food availability (Heterandria formosa -

Reznick, Callahan & Llauredo 1996; Poeciliopsis prolifica -

Banet & Reznick 2008; Poeciliopsis turneri - Banet, Au &

Reznick 2010; Phalloptychus januarius - Pollux & Reznick

2011). In all four species, we found that females are unable

to abort developing offspring. This result does not dis-

prove the Trexler-DeAngelis hypothesis, but does narrow

the range of circumstances in which the hypothesis could

apply.

In these same experiments, we also found that the

females of placental species responded to reduced food

rations by producing smaller babies, rather than aborting

some of them. In contrast, guppies, which are lecitho-

trophic, respond to a reduction in food availability by

producing larger offspring (Reznick & Yang 1993); these

offspring have a strong selective advantage to smaller off-

spring when food is scarce, but not when it is abundant

(Bashey 2006) which suggests that the production of larger

offspring in response to low food represents adaptive phe-

notypic plasticity. Prior research on a diversity of organ-

isms has yielded similar results (reviewed by Reznick &

Yang 1993). If this association between offspring size and

resource availability is general, then the production of

smaller young in response to reduced rations by all four

placental species would be maladaptive.

An alternative proposal for the evolution of placentation

is that it evolves as a by-product of intergenomic conflict

(Haig 1993; Crespi & Semeniuk 2004). The argument is

that the prior evolution of livebearing creates an enlarged

forum for parent–offspring conflict, which is driven by the

differences in what defines the fitness of parents versus off-

spring (Trivers 1974). A consequence of this difference is

that the quantity of resources that is optimal for the

embryo to get from its mother is greater than is in the best

interest of the mother to give to the embryo. The placenta

evolves as the battle front between mother and embryo, or

as the locus where there is selection on a mother’s ability

to regulate the embryo’s access to resources and on the

embryo to acquire more resources from its mother. The

possible failure of all adaptive hypotheses for the evolution

of the placenta makes this alternative explanation more

attractive to us, but what is required is positive evidence

for conflict, not a failure of all adaptive alternatives. While

there is abundant evidence for conflict in mammalian pla-

cental reproduction (e.g. Haig 1993), we have only begun

to generate evidence that addresses the conflict hypothesis

in the Poeciliidae (e.g. O’Neill et al. 2007; Schrader &

Travis 2008, 2009).

Acknowledgements

We wish to thank Yuridia Reynoso, who performed or oversaw all of the

dissections used to characterize the life histories. We would also like to

thank Alex Mamaril and Samantha Natividad for their help in the care and

maintenance of the laboratory fish populations. Doug Nelson, from the

University of Michigan Museum of Zoology, Lynn Parenti from the U. S.

National Museum, John Lundberg from the Academy of Natural Sciences

in Philadelphia and Bob Vrijenhoek generously gave us access to their col-

lections of wild-caught fishes for use in dissection and life-history character-

ization. Mariana Mateos arranged for permits to work and collect in

Mexico. This work was supported by a grant from the US National Science

Foundation (DEB-0416085).

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Received 27 June 2013; accepted 27 November 2013

Handling Editor: Charles Fox

Supporting Information

Additional Supporting information may be found in the online

version of this article:

Appendix S1. Locations and life-history values of the collections

used in the Southern clade.

Appendix S2. Log-likelihoods, Pearson’s correlation coefficients

and P-values for bivariate correlations between MI and life-

history traits in the Southern Clade.

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology

12 R. D. Bassar et al.