Life histories of poeciliid fishes: searching for a size-dependent trade-off between number and size of offspring

Abstract

A large body of knowledge about life-history traits has arisen from research on viviparous fishes of the family Poeciliidae. Still, the wide variation among species in reproductive strategies provides an excellent opportunity to further explore how life-history traits covary and the causes of covariation patterns. In this study, we provide information on brood size, offspring mass at birth, and total reproductive allotment of six poeciliid species ( Gambusia sexradiata , Poeciliopsis latidens , Poeciliopsis viriosa , Priapella intermedia , Pseudoxiphophorus jonesii , and Xiphophorus hellerii ). Also, we searched for a trade-off between the number of offspring that females produce and the size of each individual offspring. We tested the hypothesis that this trade-off should be stronger in small females because of the space constraints in the reproductive tract that are inherent to a small body size. If this hypothesis were correct, we expected a strong negative relationship between number and size of offspring in small females and a weaker or undetectable relationship between these two life-history traits in larger females. We found evidence of such a size-dependent trade-off in only one species. Small females of Po. latidens that produced relatively large broods experienced the cost of a reduction in the average size of each offspring. In larger females this negative relationship was weaker. Unexpectedly, we found no evidence of this trade-off in the other five poeciliid species and, in contrast, in one species ( Priapella intermedia ) females that produced numerous embryos were also capable of producing relatively large embryos. We discuss potential explanations for the different patterns of covariation (or lack of covariation) between number and size of offspring that we detected in these viviparous species.

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Vol.:(0123456789)
1 3
Ichthyological Research
https://doi.org/10.1007/s10228-023-00918-0
FULL PAPER
Life histories ofpoeciliid fishes: searching forasize‑dependent
trade‑off betweennumber andsize ofoffspring
J.JaimeZúñiga‑Vega1· ClaudiaOlivera‑Tlahuel2· NabilaSaleh‑Subaie1· MonserratSuárez‑Rodríguez3
Received: 17 December 2022 / Revised: 29 May 2023 / Accepted: 30 May 2023
© The Author(s) 2023
Abstract
A large body of knowledge about life-history traits has arisen from research on viviparous fishes of the family Poeciliidae.
Still, the wide variation among species in reproductive strategies provides an excellent opportunity to further explore how
life-history traits covary and the causes of covariation patterns. In this study, we provide information on brood size, off-
spring mass at birth, and total reproductive allotment of six poeciliid species (Gambusia sexradiata, Poeciliopsis latidens,
Poeciliopsis viriosa, Priapella intermedia, Pseudoxiphophorus jonesii, and Xiphophorus hellerii). Also, we searched for
a trade-off between the number of offspring that females produce and the size of each individual offspring. We tested the
hypothesis that this trade-off should be stronger in small females because of the space constraints in the reproductive tract
that are inherent to a small body size. If this hypothesis were correct, we expected a strong negative relationship between
number and size of offspring in small females and a weaker or undetectable relationship between these two life-history traits
in larger females. We found evidence of such a size-dependent trade-off in only one species. Small females of Po. latidens that
produced relatively large broods experienced the cost of a reduction in the average size of each offspring. In larger females
this negative relationship was weaker. Unexpectedly, we found no evidence of this trade-off in the other five poeciliid spe-
cies and, in contrast, in one species (Priapella intermedia) females that produced numerous embryos were also capable of
producing relatively large embryos. We discuss potential explanations for the different patterns of covariation (or lack of
covariation) between number and size of offspring that we detected in these viviparous species.
Keywords Life-history traits· Viviparous fishes· Reproductive strategies· Poeciliidae· Trade-off
Introduction
Viviparous fishes of the family Poeciliidae have been the
subject of numerous studies on a broad range of topics. From
research on these organisms, we have gained substantial
understanding of population genetics (Barson etal. 2009),
animal cognition (Cummings 2018), the origin of unisexual
species (Vrijenhoek 1994), social behavior (Krause etal.
2011), pre- and post-copulatory sexual selection (Evans
and Pilastro 2011; Rios-Cardenas and Morris 2011), biologi-
cal invasions in freshwater ecosystems (Santi etal. 2020),
the effects of environmental pollutants (Gomes-Silva etal.
2020), and cancer etiology (Schartl 2014; Lu etal. 2018).
A particular field of knowledge that has grown remarkably
from studies on poeciliid fishes is the evolution of life his-
tories (Johnson and Bagley 2011). We now know how dis-
tinct ecological factors, such as food availability, predation
intensity, and population density can cause drastic intraspe-
cific divergence in life-history traits such as age and size at
maturity, number and size of offspring, and total reproduc-
tive investment (Johnson 2001; Moore etal. 2016; Gorini-
Pacheco etal. 2018; Roth-Monzón etal. 2021). Research
on life histories of poeciliids has also provided insight into
the causes and consequences of the evolution of complex
reproductive strategies and associated morphological struc-
tures such as placentas, placentotrophy, multiple paternity,
* Monserrat Suárez-Rodríguez
monse.sr9@iztacala.unam.mx
1 Department ofEcology andNatural Resources, Faculty
ofSciences, National Autonomous University ofMexico,
University City, 04510MexicoCity, Mexico
2 Laboratory ofAnimal Behavior, Institute ofEcology,
National Autonomous University ofMexico, University City,
04510MexicoCity, Mexico
3 Faculty ofSuperior Studies Iztacala, National Autonomous
University ofMexico, 54090TlalnepantlaofBaz,
StateofMexico, Mexico

J. J. Zúñiga-Vega etal.
1 3
sperm retention, and superfetation (Olivera-Tlahuel etal.
2017; Furness etal. 2019, 2021; Dekker etal. 2022; García-
Cabello etal. 2022).
Despite the large body of knowledge on life history evolu-
tion that has arisen from studies on this group of viviparous
fishes, some aspects still deserve attention. Here, we focus
on two of these aspects. First, recent comparative studies
that analyzed the evolution of reproductive modes are based
on extensive datasets that contain species-specific values of
several life-history traits (Pollux etal. 2014; Furness etal.
2019, 2021; Reznick etal. 2021). Even though these data-
sets compiled information on numerous species, they are
not yet complete. Currently, the family Poeciliidae includes
almost 300 species (Zúñiga-Vega etal. 2022) and, according
to these datasets, life-history information is available for less
than 180 species (approximately 60% of the species in the
family). Furthermore, some life-history traits are underrep-
resented in these datasets whereas others, such as the matro-
trophy index that quantifies the amount of post-fertilization
provisioning to developing embryos, have been quantified
for a large number of poeciliid species (Furness etal. 2021).
Specifically, number of offspring produced per brood, size of
each individual offspring, and total reproductive allotment
(proportion of the female mass that is devoted to offspring
production) are three key life-history traits that have yet to
be quantified for the majority of poeciliids (Olivera-Tlahuel
etal. 2015). Additional data on these life-history traits will
allow future comparative studies on their evolution, simi-
lar to those that have been conducted on other reproductive
traits such as placentotrophy and superfetation (Pollux etal.
2014; Furness etal. 2019, 2021; García-Cabello etal. 2022).
Second, poeciliid fishes represent an excellent model
system to understand the mechanisms underlying the life-
history trade-off between number and size of offspring. Stud-
ies on some poeciliids have provided empirical evidence of
this life-history trade-off (Schrader and Travis 2012; Frías-
Alvarez etal. 2014; O’Dea etal. 2015). However, analyses
of the factors that cause this trade-off or, even more inter-
esting, of the circumstances under which this trade-off does
not occur are still needed. Pregnant females of viviparous
animals have finite space within their reproductive tract that
they can devote to offspring production (Sun etal. 2012).
Therefore, an overall increase in reproductive effort should
entail a reduction in either the number or the individual
size of their offspring (i.e., they produce either numerous
small or few large offspring; Warne and Charnov 2008).
In this case, the trade-off may arise from a morphological
constraint. However, in some animals with indeterminate
growth, such as poeciliid fishes, the volume of the reproduc-
tive tract increases hyperallometrically as they age, which
implies less space limitations in older and larger females
(Somarakis etal. 2004; Gomes and Monteiro 2008; Kharat
etal. 2008; Barneche etal. 2018). Thus, relatively old and
large females should be able to allocate energy and resources
into both number and size of young, whereas younger and
smaller reproductive females likely experience a morpholog-
ical constraint that imposes a strong offspring size-number
trade-off. To date, less than a handful of studies in fishes
have examined if this trade-off depends on the size or age of
females (Quinn etal. 2011; O’Dea etal. 2015; Lasne etal.
2018).
In this study, we contribute to the knowledge of life histo-
ries of viviparous fishes by addressing the following objec-
tives. (1) To provide quantitative information on number of
offspring produced per brood, size of each individual off-
spring, and total reproductive allotment for some members
of the family Poeciliidae for which data on these life-history
traits are still missing. (2) To test the hypothesis that the
trade-off between number and size of offspring is stronger
in small reproductive females because of the morphological
constraints associated with a small body size. Conversely,
reaching larger sizes should relieve such space restrictions,
making this trade-off undetectable in larger females.
Materials andmethods
Study species. We examined pregnant females of the follow-
ing six species of the family Poeciliidae: Gambusia sexra-
diata, Poeciliopsis latidens, Poeciliopsis viriosa, Priapella
intermedia, Pseudoxiphophorus jonesii, and Xiphophorus
hellerii. With the exception of G. sexradiata, these species
are underrepresented in the literature of poeciliid life histo-
ries (Riesch etal. 2010). Data on number of offspring (brood
size) is available for G. sexradiata, Poeciliopsis viriosa, and
X. hellerii (Reznick and Miles 1989; Riesch etal. 2010;
Pires etal. 2011), but lacking for the remaining three spe-
cies (Po. latidens, Priapella intermedia, and Pseudoxipho-
phorus jonesii). Regarding offspring size at birth, there are
quantitative reports for G. sexradiata, Poeciliopsis latidens,
Po. viriosa, and Pseudoxiphophorus jonesii (Riesch etal.
2010; Pires etal. 2011; Olivera-Tlahuel etal. 2015), whereas
the value of this life-history trait is unknown for Priapella
intermedia and X. hellerii. In turn, total reproductive allot-
ment (RA) has been quantified for G. sexradiata, Poeciliop-
sis viriosa, and X. hellerii (Reznick and Miles 1989; Riesch
etal. 2010; Pires etal. 2011), and no information of this trait
is available for the remaining three species (Po. latidens,
Priapella intermedia, and Pseudoxiphophorus jonesii).
All the preserved specimens that we examined came
from the National Collection of Fishes (Instituto de
Biología, Universidad Nacional Autónoma de México).
The particular regions (Mexican states) where females of
our six focal species were collected were (collection years
and sample sizes within parentheses): Gambusia sexra-
diata in southern Veracruz (2013, n = 42), Poeciliopsis

Size-dependent trade-off in poeciliids
1 3
latidens in central Sinaloa (2014 and 2018, n = 158),
Poeciliopsis viriosa in southern Nayarit (2013, n = 35),
Priapella intermedia in eastern Oaxaca (2012 and 2013,
n = 78), Pseudoxiphophorus jonesii in southern Veracruz
(2012 and 2013, n = 42), and Xiphophorus hellerii in east-
ern Oaxaca (2012, n = 82).
Quantification of life-history traits. We dissected pre-
served gestating females of all six species and extracted both
reproductive and digestive tracts. Before dissection, we used
a digital caliper to measure the standard length (SL) of each
female. We counted the number of developing embryos per
female and identified their stage of development according to
the classification proposed by Haynes (1995). We considered
embryos from stages 4 (recently fertilized egg) to 11 (mature
embryo). We excluded stages 1–3 because they correspond
to unfertilized ova. In the case of Poeciliopsis latidens and
Po. viriosa, which are the two species that exhibit superfeta-
tion (ability of females to bear simultaneously two or more
groups of embryos at different developmental stages; Turner
1937), we counted the number of simultaneous broods and
recorded the number of embryos contained in each brood
(i.e., the number of embryos that shared the same develop-
mental stage). All embryos and the female body were desic-
cated at 55°C during 24–48h in a drying oven. Then, the
dry mass of each embryo was estimated by dividing the dry
mass of an entire brood by the number of embryos contained
in that brood. Reproductive allotment (RA) was calculated
as the proportion of the total dry mass of the female that
consisted of developing embryos (across all broods in the
case of superfetating species):
Data analyses. We searched for a size-dependent trade-off
between number and size (dry mass) of embryos by means of
a multi-model inference approach. We implemented a set of
linear models in which we used individual embryo dry mass
as response variable (transformed to natural logarithm). For
the two species that exhibit superfetation (Po. latidens and
Po. viriosa), we used only the estimated embryo dry mass
from a single brood, which we chose randomly from each
superfetating female. In this way, we did not include more
than one data point per female in our models, thereby avoid-
ing non-independence in the data (Zúñiga-Vega etal. 2007;
Frías-Alvarez and Zúñiga-Vega 2016). However, to examine
if our results for these two species are robust regardless of
the choice of a particular brood, we also implemented all the
models that we describe below using the estimated embryo
mass from all the broods that were present in each superfe-
tating female (i.e., including more than one data point per
female; as per Zúñiga-Vega etal. 2007) as well as choosing
a different brood.
RA
=
dry mass of all embryos
female somatic dry mass
+
dry mass of all embryos .
Competing models differed in the predictor variable(s)
that could affect embryo dry mass. The main predictor var-
iable that we considered was brood size (i.e., number of
embryos per brood) and, given our hypothesis of a trade-
off, we expected a negative effect on embryo mass. A size-
dependent trade-off (stronger in small females and weaker
or non-existent in large females) was modeled by means of
an interaction between female SL and brood size affecting
embryo mass. From this model, we expected a strong nega-
tive relationship between number of embryos and individual
embryo mass in small females and a weaker relationship (a
less steep negative slope or a slope close to zero) in larger
females.
Given that developmental stage may also affect indi-
vidual embryo mass (embryo dry mass either decreases or
increases as development progresses depending on whether
the species is lecithotrophic or matrotrophic, respectively;
Marsh-Matthews 2011), we built models in which stage was
included either as the only predictor variable or in combina-
tion with other predictors (both as an additive and interac-
tive effect). In addition to the aforementioned interactive
effect of female SL and brood size, we also built a model
in which female SL was the only predictor (large females
may produce large embryos regardless of brood size and
developmental stage), models that included female SL in
combination with stage (additive and interactive effects), and
a model with an additive effect of female SL and brood size.
This latter model represents a similar offspring size-num-
ber trade-off for both small and large females, with larger
females producing larger embryos overall. Finally, we also
fitted an intercept-only model in which embryo mass was
not affected by any predictor variable. In total, we fitted 11
competing models separately for each species. The list of
models can be seen in Table1.
To select the best model for each species we used the
Akaike information criterion adjusted for small sample sizes
(AICc; Burnham and Anderson 2002). The lowest AICc
score was used to identify the model that provided the best
fit to the data. However, in those cases where two or more
models had strong support (i.e., models differing by less than
two AICc units from the best-fitting model [ΔAICc < 2]), we
selected the simpler model because the additional predictors
did not substantially improve the model fit compared to the
model with fewer parameters.
For each species, we report average values of brood
size and RA (± one standard error). The only exception
was RA of Po. viriosa because we could not obtain female
dry masses and, consequently, we were unable to quantify
this life-history trait for this species. To estimate offspring
size at birth, we predicted embryo dry mass at stage 11
(mature embryo; Haynes 1995) from the particular model
that included developmental stage as predictor with lowest
AICc score (this particular model differed among species).

J. J. Zúñiga-Vega etal.
1 3
If we detected an effect of female size on embryo mass, as
indicated by female SL being included in the best-fitting
model, we estimated offspring size at birth separately for
small and large females. For this purpose, we classified
females that measured less than the median SL as small
females and those that measured more than the median SL
as large females. Predictions of embryo mass at birth were
obtained from models on the logarithmic scale, but we back-
transformed them to the original scale (mg).
In addition, we compared among species the three life-
history traits that we studied (embryo dry mass, brood size,
and RA) accounting for the potential effect of female size on
these traits (larger species may have larger embryos, broods,
or RA; Promislow etal. 1992). For this purpose, we built
five competing linear models that we fitted separately for
each trait. These models included the following effects: (1)
differences among species with no effect of female SL, (2)
an effect of female SL without differences among species,
(3) the additive effect of species and female SL, (4) the inter-
action between species and female SL, and (5) an intercept-
only model in which the trait did not vary among species
and was not influenced by female size. As in our previous
models, embryo dry mass was transformed to natural loga-
rithm. Given that RA is a proportion, we used an arcsine
transformation (calculated as the arcsine of the square root
of the proportion) to meet the assumptions of linear mod-
els (Zar 2010). In the case of brood size, which consists
of counts of embryos, we implemented generalized linear
models with log link function and Poisson distribution (Zuur
etal. 2007). We also used AICc to select the best model
for each life-history trait. Given that average female size
differs among species (Table2) and that life-history traits
can be influenced by female size, we generated comparable
estimates of embryo mass, brood size, and RA by calculating
the expected value of these traits for a female of a common
size for all species. For this purpose, we used the average
female SL across all six species (32mm). Therefore, based
on the top model for each trait, we calculated the predicted
values of embryo mass, brood size, and RA for a female of
32mm SL of each species. These predicted size-adjusted
values were obtained on the transformed scale and then
back-transformed to their original scales (mg, number of
embryos, and proportion of total female mass, respectively).
All analyses were implemented in R version 4.1.3 (R Core
Team 2022).
Results
Size-dependent trade-off between number and size of
offspring. Only in one species, Poeciliopsis latidens, we
detected a stronger offspring size-number trade-off in small
females. For this species, the top model included the interac-
tion between female SL and brood size affecting individual
embryo dry mass (Table1). This model also included an
additive effect of developmental stage. All other models had
poor support (ΔAICc > 7 in all cases; Table1). The statisti-
cal relationship between brood size and embryo mass was
negative for both small and large females, but the negative
slope was steeper for small females (β1 = -0.020) compared
to the slope for large females (β1 = -0.013) (Fig.1a). The
relationship between developmental stage and embryo mass
was negative, indicating that embryos of Po. latidens lose
mass as development progresses (Fig.1b).
We obtained the same results for Po. latidens when using
data from all the broods present in each superfetating female
Table 1 Differences in AICc scores (ΔAICc) between each compet-
ing model and the best-fitting model (indicated by ΔAICc = 0) for six
fish species of the family Poeciliidae. In all models, the response vari-
able was embryo dry mass (transformed to natural logarithm). The
addition and multiplication symbols represent additive and interactive
effects of predictors, respectively
Models with strong support (ΔAICc < 2) are highlighted in bold
The asterisk indicates the model that we selected for each species
Model Gambusia
sexradiata Poeciliopsis
latidens Poeciliopsis
viriosa Priapella inter-
media Pseudoxiphopho-
rus jonesii Xiphopho-
rus hellerii
Intercept only 7.34 29.26 11.87 44.43 19.93 0.63*
Stage 0* 14.21 2.25 46.36 18.80 2.77
Female size 9.37 27.17 8.58 4.21 1.38* 0
Brood size 9.66 30.49 10.82 25.76 22.07 2.77
Stage + female size 1.43 7.72 0* 5.86 0.66 2.21
Stage + brood size 1.82 14.84 2.68 27.46 21.03 4.97
Female size + brood size 11.75 23.95 11.14 0* 1.05 0.63
Stage × female size 2.34 8.94 0.35 7.48 03.41
Stage × brood size 3.69 16.95 3.23 28.21 22.15 3.20
Female size × brood size 13.91 26.04 13.70 2.25 2.05 1.69
(Female size × brood size) + stage 5.40 0* 5.37 3.86 2.20 4.00

Size-dependent trade-off in poeciliids
1 3
as well as using data from a distinct brood. In both cases,
the top model indicated an interaction between female SL
and brood size affecting embryo mass as well as an additive
effect of developmental stage [Electronic Supplementary
Material (ESM) TableS1]. Also in both cases, the nega-
tive relationship between brood size and embryo mass was
stronger for small females than for large females (ESM Fig.
S1a, b) and embryos decrease in mass throughout develop-
ment (ESM Fig. S1c, d).
Additional sources of variation for embryo size. In
the other five species we did not detect a trade-off between
number and size of offspring. Instead, we found striking dif-
ferences among species in the sources of variation for indi-
vidual embryo mass. In Gambusia sexradiata three models
had strong support (ΔAICc < 2), all of which included the
effect of developmental stage (Table1). The top model only
included this predictor variable, whereas the second and
third models included female size and brood size, respec-
tively, in addition to stage. Thus, adding these two other
predictors did not substantially improve the model fit com-
pared to the model that only included the effect of stage. In
this species, embryo mass increases slightly as development
progresses (Fig.2).
In Po. viriosa, two models had strong support and both
included developmental stage and female size affecting
embryo mass (Table1). The top model indicated an addi-
tive effect of these predictors, whereas the second indi-
cated an interactive effect. We selected the former model
because it is simpler (i.e., adding the interaction term did
not substantially improve the model fit). In this species,
embryo mass decreases as development progresses and
larger females produce larger embryos overall (Fig.3).
We obtained qualitatively similar results for Po. viriosa
when analyzing data from all the broods present in each
superfetating female as well as from a different brood per
female. In both cases, the model that included an addi-
tive effect of stage and female SL provided the best fit to
the data (ESM TableS1), larger females produced larger
embryos, and embryo mass decreased throughout develop-
ment (ESM Fig. S2a, b).
In Priapella intermedia, a single model had strong sup-
port (Table1). This top model indicated an additive effect
of female size and brood size on individual embryo mass.
Contrary to our expectation, the statistical effect of brood
size on embryo mass was positive, indicating that females
that produce numerous embryos are also capable of pro-
ducing relatively large embryos (Fig.4). Also in Pr. inter-
media, larger females produce larger embryos overall. In
Pseudoxiphophorus jonesii, four models had strong sup-
port, all of which included female size as predictor vari-
able (Table1). We selected the model that only included
female size (ΔAICc = 1.38), because adding other predictors
did not improve the model fit with respect to this simpler
model. In Ps. jonesii, larger females produce noticeably
larger embryos (Fig.5). Finally, in Xiphophorus hellerii no
predictor variable had an evident effect on embryo mass as
indicated by the intercept-only model having strong support
(ΔAICc = 0.63) (Table1). Even though three other models
also had strong support (ΔAICc < 2), none of these provided
a better fit compared to the simplest intercept-only model.
Table 2 Average values of life-history traits, including female size,
for six fish species of the family Poeciliidae. In four species we
detected an effect of female size on embryo mass and, hence, we
report the predicted offspring mass at birth separately for small (S)
and large (L) females. We were unable to quantify reproductive allot-
ment for Poeciliopsis viriosa. Size-adjusted estimates account for dif-
ferences among species in average female size and were calculated
for a female of 32 mm standard length of each species
Standard errors are shown within parentheses
Species Offspring mass
at birth (mg)
Brood size
(number of
embryos)
Reproductive
allotment
Female size
(mm standard
length)
Size-adjusted estimates
Embryo dry
mass (mg)
Brood size
(number of
embryos)
Reproductive
allotment
Gambusia sexra-
diata 1.19 (0.07) 11.3 (1.21) 0.129 (0.011) 26.8 (0.62) 0.98 (0.08) 16.9 (1.02) 0.117 (0.016)
Poeciliopsis
latidens S 0.69 (0.04) 7.1 (0.37) 0.172 (0.007) 24.0 (0.27) 1.04 (0.07) 13.5 (0.82) 0.267 (0.013)
L 0.85 (0.04)
Poeciliopsis
viriosa S 0.72 (0.08) 9.6 (1.01) – 37.9 (0.79) 0.90 (0.09) 5.1 (0.51) –
L 0.82 (0.08)
Priapella inter-
media S 1.50 (0.08) 8.1 (0.49) 0.057 (0.003) 34.5 (0.52) 1.60 (0.04) 6.9 (0.34) 0.053 (0.008)
L 1.87 (0.08)
Pseudoxipho-
phorus jonesii S 1.27 (0.17) 9.7 (0.86) 0.101 (0.008) 35.2 (1.08) 1.66 (0.05) 9.1 (0.52) 0.107 (0.010)
L 2.17 (0.19)
Xiphophorus
hellerii 1.08 (0.07) 37.9 (3.22) 0.103 (0.007) 42.1 (0.93) 1.01 (0.06) 18.6 (0.66) 0.088 (0.011)

J. J. Zúñiga-Vega etal.
1 3
For illustrative purposes only, we show in Fig.6 that embryo
mass of X. hellerii does not change throughout development.
Interspecific variation in life-history traits. We
observed wide variation among species in the three life-
history traits that we examined. The smallest offspring
were observed in the two species of the genus Poeciliopsis
(between 0.69 and 0.85mg; Table2). The largest offspring
occurred in large females of Priapella intermedia (1.87mg)
and Pseudoxiphophorus jonesii (2.17mg). In five of the
six study species, mean brood sizes were relatively small
(between 7.1 and 11.3 embryos), whereas in the sixth spe-
cies (X. hellerii) females produced remarkably large broods
(37.9 embryos on average; Table2). Finally, three species
(G. sexradiata, Ps. jonesii, and X. hellerii) had relatively
similar RA (between 0.101 and 0.129; Table2). The smallest
RA was observed in Priapella intermedia (0.057) and the
largest in Poeciliopsis latidens (0.172).
Differences in female body size among species (Table2)
only partially explain the observed interspecific variation
in life-history traits. The model including the interaction
Fig. 1 Statistical effects of a brood size (number of offspring per
brood) and b developmental stage on individual embryo dry mass
(transformed to natural logarithm) of Poeciliopsis latidens. In (a), the
dashed line and white circles represent small females, whereas the
continuous line and black circles represent large females. In both (a)
and (b), the lines represent the predicted relationships according to
the model that we selected (see Table1)
Fig. 2 Statistical effect of developmental stage on individual embryo
dry mass (transformed to natural logarithm) of Gambusia sexradiata.
The dashed line represents the predicted relationship according to the
model that we selected (see Table1)
Fig. 3 Statistical effect of developmental stage on individual embryo
dry mass (transformed to natural logarithm) of Poeciliopsis viriosa.
The dashed line and white circles represent small females, whereas
the continuous line and black circles represent large females. Both
lines represent the predicted relationships according to the model that
we selected (see Table1)

Size-dependent trade-off in poeciliids
1 3
between species and female SL unambiguously provided
the best fit to all three traits (Table3), indicating that the
influence of female size on embryo mass, brood size, and
RA differed among species (Fig.7). Despite being medium-
sized species, Priapella intermedia and Pseudoxiphophorus
jonesii produce the largest embryos (Fig.7a). In the case of
number of offspring, the largest broods are indeed produced
by the largest species, X. hellerii (Fig.7b). In contrast, the
greatest RA occurred in the smallest species, Poeciliopsis
latidens (Fig.7c). Size-adjusted estimates of these traits
also confirmed that, for a female of the same size (32mm
SL), Priapella intermedia and Pseudoxiphophorus jonesii
produce the largest embryos, X. hellerii produces the larg-
est broods, and Poeciliopsis latidens has the greatest RA
(Table2). In addition, size-adjusted estimates also revealed
Fig. 4 Statistical effect of brood size (number of offspring per brood)
on individual embryo dry mass (transformed to natural logarithm)
of Priapella intermedia. The dashed line and white circles represent
small females, whereas the continuous line and black circles represent
large females. Both lines represent the predicted relationships accord-
ing to the model that we selected (see Table1)
Fig. 5 Statistical effect of female size on individual embryo dry mass
(transformed to natural logarithm) of Pseudoxiphophorus jonesii.
The dashed line represents the predicted relationship according to the
model that we selected (see Table1)
Fig. 6 Individual embryo dry mass (transformed to natural logarithm)
of Xiphophorus hellerii plotted against developmental stage. The
dashed line represents the predicted effect of developmental stage
according to the model that only included this predictor. Notice that
embryo mass remains relatively constant throughout development
Table 3 Differences in AICc scores (ΔAICc) between each compet-
ing model and the best-fitting model (indicated by ΔAICc = 0 and
highlighted in bold) for three life-history traits of six fish species of
the family Poeciliidae. Competing models represent that traits may
vary among species and/or may be influenced by female size. The
addition and multiplication symbols represent additive and interactive
effects of predictors, respectively
Model Embryo dry mass Brood size Reproduc-
tive allot-
ment
Intercept only 308.96 4310.22 177.36
Species 67.76 1020.24 45.39
Female size 250.74 966.84 157.31
Species + female size 27.15 58.58 33.64
Species × female size 0 0 0

J. J. Zúñiga-Vega etal.
1 3
that, despite their small sizes, females of both G. sexradiata
and Po. latidens produce relatively large broods (Table2).
Discussion
We have provided a series of quantitative information on
brood size, offspring mass at birth, and reproductive allot-
ment in Poeciliopsis latidens, Priapella intermedia, Pseu-
doxiphophorus jonesii, and Xiphophorus hellerii of the fam-
ily Poeciliidae for which data on these life-history traits were
still missing. In addition, we have provided evidence of a
size-dependent trade-off between number and size of off-
spring in one of the six species that we studied. Females of
Poeciliopsis latidens that produce more embryos do so at the
cost of a reduction in the size of each embryo. This trade-off
occurred in both small and large females of this species, but
was stronger in the former. This pattern suggests that in this
species, morphological constraints occur all throughout their
life cycles, but are more severe in the early phases of adult-
hood. As females grow, such space limitations are relaxed
slightly and the offspring size-number trade-off becomes
less strong. However, we must notice here that we hypoth-
esized that the trade-off should not exist or at least should
be undetectable in large females, which is a pattern that did
not occur in Po. latidens. Instead, the trade-off still persists
as females grow, although to a lesser extent.
The body shape of species of the genus Poeciliopsis
is relatively thin and fusiform (Zúñiga-Vega etal. 2007;
Frías-Alvarez and Zúñiga-Vega 2016; Fleuren etal. 2018),
compared to members of other poeciliid genera, which in
general have deeper bodies (Gomes and Monteiro 2008;
Zúñiga-Vega etal. 2011; Johnson etal. 2014). This particu-
lar morphology could explain why the offspring size-number
trade-off still occurs in larger females, despite their larger
body size and concomitant larger reproductive cavity. In
other words, a fusiform body shape likely imposes space
restrictions on all body sizes. However, this explanation is
not consistent with the absence of this trade-off in the con-
generic Po. viriosa, which also has a relatively thin mor-
phology. An alternative explanation is a difference between
species in food availability. The occurrence of trade-offs
may depend on the external conditions rather than on (or
in addition to) the intrinsic characteristics of the species
(van Noordwijk and de Jong 1986). In particular, environ-
ments where food is abundant may allow females to acquire
enough energetic reserves to produce numerous embryos
without a detrimental effect on their individual size (Zera
and Harshman 2001; Blanckenhorn and Heyland 2004). In
contrast, low food availability entails energetic restrictions
for females, which in turn impedes the allocation of nutri-
ents to both number and size of embryos (Stahlschmidt and
Adamo 2015; Mishra and Kumar 2019). Therefore, our col-
lections of Po. viriosa may have come from a population
where food is abundant and, in contrast, the females of Po.
latidens that we examined may have come from a population
Fig. 7 Statistical effects of female size on a individual embryo dry
mass (transformed to natural logarithm), b brood size (also trans-
formed to natural logarithm), and c reproductive allotment (trans-
formed to arcsine square-root values) for six fish species of the family
Poeciliidae. Fitted lines were derived from models that included the
interaction between species and female size affecting each trait. The
length of the lines represents the range of female sizes of each species

Size-dependent trade-off in poeciliids
1 3
where food is scarce. In addition, differences in female body
size between Po. latidens and Po. viriosa can also explain
the occurrence of this trade-off only in Po. latidens because
females of Po. viriosa are substantially larger (37.9mm
SL on average) than females of Po. latidens (24.0mm SL
on average; Table2). A larger body size provides a larger
reproductive cavity and, hence, less space restrictions for
offspring production (Saleh-Subaie etal. 2021).
Interestingly, we did not detect the offspring size-number
trade-off in the other four species, suggesting a lack of mor-
phological restrictions and/or abundant food sources. Three
of these species (Priapella intermedia, Pseudoxiphopho-
rus jonesii, and X. hellerii) have relatively large body sizes
(see Table2) and, therefore, larger reproductive tracts and
looser constraints on offspring size and brood size. In fact,
in Priapella intermedia, we detected a positive relationship
between number and size of embryos, which is opposite to
what we expected. This means that some females of this
species are able to produce numerous large embryos. This
ability may come from the relatively deep body of mem-
bers of the genus Priapella (Riesch etal. 2012), which pro-
vides females with ample space within their reproductive
cavities. In poeciliid fishes, morphology can indeed exert
strong pressures on reproductive investment (Ghalambor
etal. 2004; Quicazan-Rubio etal. 2019). Opposite to the
apparent lack of morphological restrictions that we observed
in Pr. intermedia, other species of this family have narrow
bodies that impose limits on the number and size of young
that females can produce. For instance, Alfaro cultratus has
a narrow body and keeled ventral surface that apparently
have impeded the evolution of increased reproductive allot-
ment even in the presence of strong selective pressures that
promote increased fecundity (e.g., in high-predation envi-
ronments; Golden etal. 2021). Another interesting example
of morphological constraints on reproduction is superfeta-
tion, which is a reproductive strategy that could have arisen
in poeciliid fishes as an adaptive response to environments
that favor streamlined morphologies (e.g., fast-flowing riv-
ers; Zúñiga-Vega etal. 2010). Apparently, superfetation
allows females to have high fecundities without substantial
increases in the volume of their abdomens (Zúñiga-Vega
etal. 2007, 2017; Fleuren etal. 2019).
Our findings also revealed that in four species (Poe-
ciliopsis latidens, Po. viriosa, Priapella intermedia, and
Pseudoxiphophorus jonesii) larger females produce larger
embryos. A large size at birth can be advantageous under
different ecological conditions. In environments with intense
intraspecific competition, larger offspring of the least killi-
fish (Heterandria formosa) and guppies (Poecilia reticulata)
are better competitors and have higher fitness than smaller
ones (Bashey 2008; Schrader and Travis 2012). In water
bodies that contain toxic compounds such as hydrogen
sulfide, a large size at birth confers a low surface/volume
ratio and, consequently, less surface area per volume of body
tissue is exposed to the toxins (Riesch etal. 2010). Large
offspring likely have relatively low metabolic rates and,
thus, low oxygen consumption, which could be beneficial
in aquatic environments with low dissolved oxygen (Riesch
etal. 2010). Moreover, intense cannibalism on juveniles also
selects for larger offspring sizes, as documented in Poecili-
opsis monacha (Thibault 1974; Weeks and Gaggiotti 1993).
In numerous animal species, natural selection favors a large
female size, which has been mostly explained as a result of
the greater fecundity (i.e., larger broods) associated with
a larger body (Cox etal. 2003; Lim etal. 2014; Pincheira-
Donoso and Hunt 2017). Our findings indicate that, in some
poeciliid species, a larger female size also conveys the selec-
tive advantage of larger newborns.
Larger females may also be capable of producing more
embryos per brood (Zúñiga-Vega etal. 2011; Barneche
etal. 2018) and our data confirms this positive relationship
between female size and fecundity in five of our study spe-
cies (with the exception of Pseudoxiphophorus jonesii; see
Fig.7b). At the interspecific level, we also observed this
same pattern: the largest broods were produced by the largest
species, X. hellerii. Directional selection for larger female
size due to the fitness benefit of producing numerous off-
spring has been demonstrated in several taxa (Lefranc and
Bundgaard 2000; Fox and Czesak 2006; Nali etal. 2014).
Intriguingly, in all but one species reproductive allotment
did not increase with female size (the only exception was
Poeciliopsis latidens; see Fig.7c), which indicates that even
though females can increase the number and/or size of their
offspring as they grow, the relative amount of energy that
they invest in reproduction (relative with respect to their
body size) remains constant throughout their lives. This
unexpected finding suggests that a disproportionately greater
reproductive investment by larger females may not result
in a significant increase in the fitness of their young (i.e.,
may not increase the number of offspring surviving to sexual
maturity). Instead, a disproportionately greater reproductive
allotment may impose physiological costs. Interestingly, the
only species in which reproductive allotment increased with
female size was the same species in which we detected the
trade-off between number and size of offspring, Po. latidens.
Our data for this species indicate that large females of Po.
latidens make a disproportionately greater reproductive
investment through larger broods at the cost of a reduction
in the size of each individual offspring.
Our study revealed three patterns of covariation among
female size, number of offspring per brood, and embryo
mass in poeciliid fishes. These distinct life-history strate-
gies are likely shaped by ecological factors (both biotic and
abiotic) and biological constraints. First, in three species
(Po. latidens, Po. viriosa, and Priapella intermedia) both
brood size and embryo mass increased with female size.

J. J. Zúñiga-Vega etal.
1 3
Presumably, these species inhabit environments with high
mortality rates that select for greater fecundity (Reznick
etal. 1996), intense intraspecific competition that promotes
large offspring size (Bashey 2008), and abundant food
sources that allow females to simultaneously invest in both
number and size of offspring (Taborsky 2006). Second, in
two species (Gambusia sexradiata and X. hellerii) fecundity
increases with female size whereas offspring mass remains
invariant regardless of maternal size. Selection pressure for
an optimal offspring size at birth may be strong in the habi-
tats of these two species (Jørgensen etal. 2011). Another
possibility is that smaller offspring are not viable and, hence,
females are not able to further reduce offspring size in order
to increase brood size (this is another plausible explanation
for why the offspring size-number trade-off does not occur in
these species). Alternatively, offspring size could be geneti-
cally constrained. Third, in one species (Pseudoxiphophorus
jonesii) larger females produce larger embryos but brood
size does not increase with female size. In this case, females
may experience selection against a distended abdomen as a
result of fast water currents or high predation risk, which
are ecological conditions that impose strong pressures on
swimming performance (Zúñiga-Vega etal. 2007; Wesner
etal. 2011; Ingley etal. 2014). High fecundity entails a sub-
stantial increase in abdomen volume, which has a negative
impact on swimming performance (Ghalambor etal. 2004;
Quicazan-Rubio etal. 2019). Thus, a small brood size allows
females of Ps. jonesii to maintain a less distended abdomen
during pregnancy and, therefore, an efficient swimming per-
formance. All these tentative explanations represent hypoth-
eses that require empirical research.
In general, previous reports of the mode of maternal pro-
visioning to developing embryos are not consistent with our
findings. Specifically, Poeciliopsis viriosa has been considered
as having incipient matrotrophy (Pollux etal. 2014; Furness
etal. 2019, 2021), whereas the negative relationship between
developmental stage and embryo mass that we observed in this
species indicates that females rely entirely on yolk for embryo
nutrition, without post-fertilization provisioning (i.e., strict
lecithotrophy). In lecithotrophic species, embryo dry mass
decreases throughout development due to metabolic costs
(Reznick etal. 2002; Marsh-Matthews 2011). Furthermore, G.
sexradiata, Priapella intermedia, Pseudoxiphophorus jonesii,
and X. hellerii were previously considered as lecithotrophic
(Furness etal. 2019, 2021), whereas in contrast our results
suggest that these species are moderately matrotrophic (in the
case of G. sexradiata) or at least capable of incipient matro-
trophy (in the cases of Priapella intermedia, Pseudoxipho-
phorus jonesii, and X. hellerii). In G. sexradiata evidence of
moderate matrotrophy comes from embryos increasing mod-
erately in mass throughout development, which indicates that
females actively transfer nutrients to embryos during gesta-
tion (Reznick etal. 2002; Marsh-Matthews 2011). In Priapella
intermedia, Pseudoxiphophorus jonesii, and X. hellerii evi-
dence of incipient matrotrophy comes from a lack of relation-
ship between stage and embryo mass (depicted in Fig.6 for X.
hellerii), which indicates that embryos maintain a constant dry
mass throughout development. In species with incipient matro-
trophy, embryos feed mainly on yolk but obtain small amounts
of nutrients directly from females during gestation, thereby
offsetting the metabolic costs that otherwise would cause a
reduction in embryo dry mass (Marsh-Matthews etal. 2001;
Reznick etal. 2002; Pollux etal. 2009). The only exception
was Poeciliopsis latidens because both our data and previous
reports indicate that this species is lecithotrophic (Pollux etal.
2014; Furness etal. 2019, 2021).
Differences between studies can be explained by intraspe-
cific variation in the mode of maternal provisioning to devel-
oping embryos, which in turn could arise from environmental
effects on the relative amounts of pre- and post-fertilization
sources of embryonic nourishment. There is now solid evi-
dence that increased amounts of post-fertilization provision-
ing (i.e., higher degrees of matrotrophy) can be advantageous
under particular conditions (e.g., where food is abundant or
predation risk is high; Riesch etal. 2013; Gorini-Pacheco etal.
2018; Hagmayer etal. 2020) and that females of some poecil-
iid species can facultatively increase or decrease the nutrients
that they actively transfer to embryos during gestation depend-
ing on the external conditions (specifically depending on food
availability; Pires etal. 2007; Molina-Moctezuma etal. 2020).
Supplementary Information The online version contains supplemen-
tary material available at https:// doi. org/ 10. 1007/ s10228- 023- 00918-0.
Acknowledgments Funding was provided by Consejo Nacional de
Ciencia y Tecnología, México (CONACyT) through grant number
129675. We thank Israel Solano-Zavaleta, Mariana Hernández-Apoli-
nar, Marco Romero-Romero, and Pedro Mendoza-Hernández for pro-
viding technical assistance.
Declarations
Conflicts of interest All authors declare that they do not have conflict
of interests.
Ethics approval No ethics approval required because this research was
based on museum specimens.
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article's Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article's Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.

Size-dependent trade-off in poeciliids
1 3
References
Barneche DR, Robertson DR, White CR, Marshall DJ (2018) Fish
reproductive-energy output increases disproportionately with
body size. Science 360:642–645
Barson NJ, Cable J, van Oosterhout C (2009) Population genetic analy-
sis of microsatellite variation of guppies (Poecilia reticulata) in
Trinidad and Tobago: evidence for a dynamic source-sink meta-
population structure, founder events and population bottlenecks.
J Evol Biol 22:485–497
Bashey F (2008) Competition as a selective mechanism for larger off-
spring size in guppies. Oikos 117:104–113
Blanckenhorn WU, Heyland A (2004) The quantitative genetics of two
life history trade-offs in the yellow dung fly in abundant and lim-
ited food environments. Evol Ecol 18:385–402
Burnham KP, Anderson DR (2002) Model selection and multimodel
inference. A practical information-theoretic approach, 2nd edn.
Springer, New York
Cox RM, Skelly SL, John-Alder HB (2003) A comparative test of adap-
tive hypotheses for sexual size dimorphism in lizards. Evolution
57:1653–1669
Cummings ME (2018) Sexual conflict and sexually dimorphic cogni-
tion—reviewing their relationship in poeciliid fishes. Behav Ecol
Sociobiol 72:73
Dekker ML, van Son LM, Leon-Kloosterziel KM, Hagmayer A, Fur-
ness AI, van Leeuwen JL, Pollux BJ (2022) Multiple paternity in
superfetatious live-bearing fishes. J Evol Biol 35:948–961
Evans JP, Pilastro A (2011) Postcopulatory sexual selection. In: Evans
JP, Pilastro A, Schlupp I (eds) Ecology and evolution of poeciliid
fishes. The University of Chicago Press, Chicago, pp 197–208
Fleuren M, Quicazan-Rubio EM, van Leeuwen JL, Pollux BJA
(2018) Why do placentas evolve? Evidence for a morphologi-
cal advantage during pregnancy in live-bearing fish. PLoS One
13:e0195976
Fleuren M, van Leeuwen JL, Pollux BJA (2019) Superfetation reduces
the negative effects of pregnancy on the fast-start escape perfor-
mance in live-bearing fish. Proc R Soc B Biol Sci 286:20192245
Fox CW, Czesak ME (2006) Selection on body size and sexual size
dimorphism differs between host species in a seed-feeding beetle.
J Evol Biol 19:1167–1174
Frías-Alvarez P, Macías Garcia C, Vázquez-Vega L, Zúñiga-Vega J
(2014) Spatial and temporal variation in superfoetation and related
life history traits of two viviparous fishes: Poeciliopsis gracilis
and P. infans. Naturwissenschaften 101:1085–1098
Frías-Alvarez P, Zúñiga-Vega JJ (2016) Superfetation in live-bearing
fishes is not always the result of a morphological constraint. Oeco-
logia 181:645–658
Furness AI, Avise JC, Pollux BJA, Reynoso Y, Reznick DN (2021)
The evolution of the placenta in poeciliid fishes. Curr Biol
31:2004–2011
Furness AI, Pollux BJA, Meredith RW, Springer MS, Reznick DN
(2019) How conflict shapes evolution in poeciliid fishes. Nat
Commun 10:3335
García-Cabello KN, Fuentes-González JA, Saleh-Subaie N, Pienaar J,
Zúñiga-Vega JJ (2022) Increased superfetation precedes the evolu-
tion of advanced degrees of placentotrophy in viviparous fishes of
the family Poeciliidae. Biol Lett 18:20220173
Ghalambor CK, Reznick DN, Walker JA (2004) Constraints on adap-
tive evolution: the functional trade-off between reproduction
and fast-start swimming performance in the Trinidadian guppy
(Poecilia reticulata). Am Nat 164:38–50
Golden KB, Belk MC, Johnson JB (2021) Predator environment does
not predict life history in the morphologically constrained fish
Alfaro cultratus (Cyprinodontiformes: Poeciliidae). Front Ecol
Evol 9:607802
Gomes JL, Monteiro LR (2008) Morphological divergence patterns
among populations of Poecilia vivipara (Teleostei Poeciliidae):
test of an ecomorphological paradigm. Biol J Linn Soc Lond
93:799–812
Gomes-Silva G, Pereira BB, Liu K, Chen B, Santos VSV, de Men-
ezes GHT, Pires LP, Santos BMT, Oliveira DM, Alves Machado
PH, de Oliveira Júnior RJ, Machado de Oliveira AM, Plath M
(2020) Using native and invasive livebearing fishes (Poeciliidae,
Teleostei) for the integrated biological assessment of pollution in
urban streams. Sci Total Environ 698:134336
Gorini-Pacheco B, Zandonà E, Mazzoni R (2018) Predation effects on
matrotrophy, superfetation and other life history traits in Phal-
loceros harpagos. Ecol Freshw Fish 27:442–452
Hagmayer A, Furness AI, Reznick DN, Dekker ML, Pollux BJ (2020)
Predation risk shapes the degree of placentation in natural popula-
tions of live-bearing fish. Ecol Lett 23:831–840
Haynes JL (1995) Standardized classification of poeciliid development
for life-history studies. Copeia 1995:147–154
Ingley SJ, Billman EJ, Belk MC, Johnson JB (2014) Morphological
divergence driven by predation environment within and between
species of Brachyrhaphis fishes. PLoS One 9:e90274
Johnson JB (2001) Adaptive life-history evolution in the livebearing
fish Brachyrhaphis rhabdophora: genetic basis for parallel diver-
gence in age and size at maturity and a test of predator-induced
plasticity. Evolution 55:1486–1491
Johnson JB, Bagley JC (2011) Ecological drivers of life-history diver-
gence. In: Evans JP, Pilastro A, Schlupp I (eds) Ecology and
evolution of poeciliid fishes. The University of Chicago Press,
Chicago, pp 38–49
Johnson JB, Macedo DC, Passow CN, Rosenthal GG (2014) Sexual
ornaments, body morphology, and swimming performance in
naturally hybridizing swordtails (Teleostei: Xiphophorus). PLoS
One 9:109025
Jørgensen C, Auer SK, Reznick DN (2011) A model for optimal off-
spring size in fish, including live-bearing and parental effects. Am
Nat 177:E119–E135
Kharat SS, Khillare YK, Dahanukar N (2008) Allometric scaling
in growth and reproduction of a freshwater loach Nemacheilus
mooreh (Sykes, 1839). Electron J Ichthyol 4:8–17
Krause J, James R, Croft DP (2011) Group living. In: Evans JP, Pilastro
A, Schlupp I (eds) Ecology and evolution of poeciliid fishes. The
University of Chicago Press, Chicago, pp 145–154
Lasne E, Leblanc CA-L, Gillet C (2018) Egg size versus number of
offspring trade-off: female age rather than size matters in a domes-
ticated Arctic charr population. Evol Biol 45:105–112
Lefranc A, Bundgaard J (2000) The influence of male and female body
size on copulation duration and fecundity in Drosophila mela-
nogaster. Hereditas 132:243–247
Lim JN, Senior AM, Nakagawa S (2014) Heterogeneity in individual
quality and reproductive trade-offs within species. Evolution
68:2306–2318
Lu Y, Boswell M, Boswell W, Kneitz S, Hausmann M, Klotz B, Regn-
eri J, Savage M, Amores A, Postlethwait J, Warren W, Schartl M,
Walter R (2018) Comparison of Xiphophorus and human mela-
noma transcriptomes reveals conserved pathway interactions. Pig-
ment Cell Melanoma Res 31:496–508
Marsh-Matthews E (2011) Matrotrophy. In: Evans JP, Pilastro A, Sch-
lupp I (eds) Ecology and evolution of poeciliid fishes. The Uni-
versity of Chicago Press, Chicago, pp 18–27
Marsh-Matthews E, Skierkowski P, DeMarais A (2001) Direct evidence
for mother-to-embryo transfer of nutrients in the livebearing fish
Gambusia geiseri. Copeia 2001:1–6

J. J. Zúñiga-Vega etal.
1 3
Mishra I, Kumar V (2019) The quantity–quality trade-off: differential
effects of daily food availability times on reproductive perfor-
mance and offspring quality in diurnal zebra finches. J Exp Biol
222:jeb196667
Molina-Moctezuma A, Hernández-Rosas AL, Zúñiga-Vega JJ (2020)
Resource availability and its effects on mother to embryo nutrient
transfer in two viviparous fish species. J Exp Zool A Ecol Integr
Physiol 333:181–193
Moore MP, Riesch R, Martin RA (2016) The predictability and magni-
tude of life-history divergence to ecological agents of selection: a
meta-analysis in livebearing fishes. Ecol Lett 19:435–442
Nali RC, Zamudio KR, Haddad CFB, Prado CPA (2014) Size-depend-
ent selective mechanisms on males and females and the evolution
of sexual size dimorphism in frogs. Am Nat 184:727–740
O’Dea RE, Vega-Trejo R, Head ML, Jennions MD (2015) Maternal
effects on offspring size and number in mosquitofish, Gambusia
holbrooki. Ecol Evol 5:2945–2955
Olivera-Tlahuel C, Ossip-Klein AG, Espinosa-Pérez HS, Zúñiga-Vega
JJ (2015) Have superfetation and matrotrophy facilitated the evo-
lution of larger offspring in poeciliid fishes? Biol J Linn Soc Lond
116:787–804
Olivera-Tlahuel C, Villagrán-Santa Cruz M, Moreno-Mendoza NA,
Zúñiga-Vega JJ (2017) Morphological structures for potential
sperm storage in poeciliid fishes. Does superfetation matter? J
Morphol 278:907–918
Pincheira-Donoso D, Hunt J (2017) Fecundity selection theory: con-
cepts and evidence. Biol Rev Camb Philos Soc 92:341–356
Pires MN, Bassar RD, McBride KE, Regus JU, Garland Jr T, Reznick
DN (2011) Why do placentas evolve? An evaluation of the life-
history facilitation hypothesis in the fish genus Poeciliopsis. Funct
Ecol 25:757–768
Pires MN, McBride KE, Reznick DN (2007) Interpopulation variation
in life-history traits of Poeciliopsis prolifica: implications for the
study of placental evolution. J Exp Zool A Ecol Genet Physiol
307:113–125
Pollux BJA, Meredith RW, Springer MS, Garland T, Reznick DN
(2014) The evolution of the placenta drives a shift in sexual selec-
tion in livebearing fish. Nature 513:233–236
Pollux BJA, Pires MN, Banet AI, Reznick DN (2009) Evolution of
placentas in the fish family Poeciliidae: an empirical study of mac-
roevolution. Annu Rev Ecol Evol Syst 40: 271–289
Promislow D, Clobert J, Barbault R (1992) Life history allometry
in mammals and squamate reptiles: taxon-level effects. Oikos
65:285–294
Quicazan-Rubio EM, Van Leeuwen JL, Van Manen K, Fleuren M,
Pollux BJ, Stamhuis EJ (2019) Coasting in live-bearing fish: the
drag penalty of being pregnant. J R Soc Interface 16:20180714
Quinn TP, Seamons TR, Vollestad LA, Duffy E (2011) Effects of
growth and reproductive history on the egg size-fecundity trade-
off in steelhead. Trans Am Fish Soc 140:45–51
R Core Team (2022) R: a language and environment for statistical com-
puting. R Foundation for Statistical Computing, Vienna, Austria.
https:// www.r- proje ct. org/
Reznick DN, Butler MJ, Rodd FH, Ross P (1996) Life‐history evolu-
tion in guppies (Poecilia reticulata) 6. Differential mortality as a
mechanism for natural selection. Evolution 50:1651–1660
Reznick DN, Mateos M, Springer MS (2002) Independent origins and
rapid evolution of the placenta in the fish genus Poeciliopsis. Sci-
ence 298:1018–1020
Reznick DN, Miles DB (1989) Review of life history patterns in poe-
ciliid fishes. In: Meffe GK, Snelson FF (eds) Ecology and evolu-
tion of livebearing fishes (Poeciliidae). Prentice Hall, Englewood
Cliffs, pp 125–148
Reznick DN, Travis J, Pollux BJA, Furness AI (2021) Reproductive
mode and conflict shape the evolution of male attributes and
rate of speciation in the fish family Poeciliidae. Front Ecol Evol
9:639751
Riesch R, Martin RA, Bierbach D, Plath M, Langerhans RB, Arias-
Rodriguez L (2012) Natural history, life history, and diet of Pria-
pella chamulae Schartl, Meyer & Wilde 2006 (Teleostei: Poecili-
idae). Aqua Int J Ichthyol 18:95–102
Riesch R, Martin RA, Langerhans RB (2013) Predation’s role in life-
history evolution of a livebearing fish and a test of the Trexler-
DeAngelis model of maternal provisioning. Am Nat 181:78–93
Riesch R, Plath M, García de León FJ, Schlupp I (2010) Convergent
life-history shifts: toxic environments result in big babies in two
clades of poeciliids. Naturwissenschaften 97:133–141
Rios-Cardenas O, Morris MR (2011) Precopulatory sexual selection.
In: Evans JP, Pilastro A, Schlupp I (eds) Ecology and evolution
of poeciliid fishes. The University of Chicago Press, Chicago,
pp 187–196
Roth-Monzón AJ, Belk MC, Zúñiga-Vega JJ, Johnson JB (2021)
What drives life-history variation in the livebearing fish Poecili-
opsis prolifica? An assessment of multiple putative selective
agents. Front Ecol Evol 8:608046
Saleh-Subaie N, Johnson JB, Zúñiga-Vega JJ (2021) Small sizes, big
strategies: the relationship between female size, matrotrophy
and superfetation throughout the reproductive lives of poeciliid
fishes. J Zool 315:261–275
Santi F, Riesch R, Baier J, Grote M, Hornung S, Jüngling H, Plath
M, Jourdan J (2020) A century later: adaptive plasticity and
rapid evolution contribute to geographic variation in invasive
mosquitofish. Sci Total Environ 726:137908
Schartl M (2014) Beyond the zebrafish: diverse fish species for mod-
eling human disease. Dis Model Mech 7:181–192
Schrader M, Travis J (2012) Assessing the roles of population den-
sity and predation risk in the evolution of offspring size in popu-
lations of a placental fish. Ecol Evol 2:1480–1490
Somarakis S, Ganias K, Tserpes G, Koutsikopoulos C (2004) Ovar-
ian allometry and the use of the gonosomatic index: a case
study in the Mediterranean sardine, Sardina pilchardus. Mar
Biol 146:181–189
Stahlschmidt ZR, Adamo SA (2015) Food-limited mothers favour
offspring quality over offspring number: a principal components
approach. Funct Ecol 29:88–95
Sun YY, Du Y, Yang J, Fu TB, Lin CX, Ji X (2012) Is the evolution
of viviparity accompanied by a relative increase in maternal
abdomen size in lizards? Evol Biol 39:388–399
Taborsky B (2006) The influence of juvenile and adult environments
on life-history trajectories. Proc R Soc B Biol Sci 273:741–750
Thibault RE (1974) Genetics of cannibalism in a viviparous fish
and its relationship to population density. Nature 251:138–140
Turner CL (1937) Reproductive cycles and superfetation in poeciliid
fishes. Biol Bull 72:145–164
van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of
resources: their influence on variation in life history tactics. Am
Nat 128:137–142
Vrijenhoek RC (1994) Unisexual fish: model systems for studying
ecology and evolution. Annu Rev Ecol Syst 25:71–96
Warne RW, Charnov EL (2008) Reproductive allometry and the size-
number trade-off for lizards. Am Nat 172:E80–E98
Weeks SC, Gaggiotti OE (1993) Patterns of offspring size at birth in
clonal and sexual strains of Poeciliopsis (Poeciliidae). Copeia
1993:1003–1009
Wesner JS, Billman EJ, Meier A, Belk MC (2011) Morphological
convergence during pregnancy among predator and nonpredator
populations of the livebearing fish Brachyrhaphis rhabdophora
(Teleostei: Poeciliidae). Biol J Linn Soc Lond 104:386–392
Zar JH (2010) Biostatistical analysis, fifth edition. Pearson Prentice
Hall, Upper Saddle River

Size-dependent trade-off in poeciliids
1 3
Zera AJ, Harshman LG (2001) The physiology of life history trade-
offs in animals. Annu Rev Ecol Syst 32:95–126
Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data.
Springer, New York
Zúñiga-Vega JJ, Aspbury AS, Johnson JB, Pollux BJA (2022) Edito-
rial: ecology, evolution, and behavior of viviparous fishes. Front
Ecol Evol 10:832216
Zúñiga-Vega JJ, Macías-Garcia C, Johnson JB (2010) Hypotheses
to explain the evolution of superfetation in viviparous fishes.
In: Uribe MC, Grier HJ (eds) Viviparous fishes II. New Life
Publications, Homestead, pp 241–254
Zúñiga-Vega JJ, Olivera-Tlahuel C, Molina-Moctezuma A (2017)
Superfetation increases total fecundity in a viviparous fish regard-
less of the ecological context. Acta Oecol 84:48–56
Zúñiga-Vega JJ, Reznick DN, Johnson JB (2007) Habitat predicts
reproductive superfetation and body shape in the livebearing fish
Poeciliopsis turrubarensis. Oikos 116:995–1005
Zúñiga-Vega JJ, Suárez-Rodríguez M, Espinosa-Pérez H, Johnson
JB (2011) Morphological and reproductive variation among
populations of the Pacific molly Poecilia butleri. J Fish Biol
79:1029–1046
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