Benefits and drawbacks of the placenta in live-bearing fish

Understanding the evolution of complex traits is of fundamental interest to scientists and non-scientists alike. The placenta is an excellent example of a complex trait that has evolved repeatedly throughout the animal kingdom. This repeated evolution and ongoing elaboration appears to point towards an adaptive advantage to specific environmental conditions; however, this potential benefit is currently insufficiently understood. In this thesis, I attempt to shed light on the causes and consequences of placental evolution by drawing on insights from the live-bearing fish family Poeciliidae.In Chapter 2, we studied maternal causes and consequences of embryo provisioning during gestation in the placental live-bearing fish species Poeciliopsis retropinna from Costa Rica. Specifically, we examined how maternal traits (i.e. body fat, lean mass, and length) relate to pre- (allocation to eggs prior to fertilization) and post-fertilization (allocation to embryos during pregnancy) maternal provisioning and how this ultimately affects offspring size and body composition at birth. We showed that maternal traits strongly, albeit differently, correlate with embryo size and body composition throughout pregnancy. We conclude that (i) embryo size and offspring size at birth are plastic phenotypic traits predicted by the maternal phenotype, and (ii) maternal provisioning is not constant throughout pregnancy, but depends on the embryo developmental stage.In Chapter 3, we studied natural populations of the placental live-bearing fish species P. retropinna in Costa Rica to test a key prediction of the locomotor cost hypothesis, which is that the placenta evolves in high ‘performance-demanding’ environments by gradually shifting maternal investment from pre- to post-fertilization, thereby reducing the reproductive burden experienced by females during pregnancy and improving their locomotor performance. We confirmed two key predictions of this hypothesis, which are that (i) placentas evolve in natural populations in response to high predation and (ii) that this significantly reduces a female’s reproductive burden during pregnancy. This chapter provides the first evidence for an adaptive explanation for why the placenta evolves in natural populations. Moreover, it reveals an unexpected fundamental feature of placental animals, which is that an increase in the degree of placentation can lead to a lower reproductive burden without any apparent reproductive cost: i.e. without sacrificing either fecundity or offspring size and quality at birth.In Chapter 4, we tested the idea that placentation and superfetation reduce the reproductive burden of females during pregnancy, facilitating life in ‘performance-demanding’ (micro)habitats. If true, then placental and/or superfetatious species should be able to inhabit higher performance-demanding (micro)habitats compared to closely related non-placental and/or non-superfetatious species. For this, we used underwater visual census to study diurnal and ontogenetic microhabitat selection in Costa Rican rivers by five sympatric live-bearing fish species (family Poeciliidae) that differ in the absence/presence of placentation and superfetation. Consistent with the theory, adults of placental and superfetatious species inhabited deep and fast-flowing water, species that lack both reproductive adaptations were confined to shallow and slow-flowing areas, and species that lack a placenta but have superfetation occupied an intermediate habitat. This interspecific daytime microhabitat use was strongest in reproductive adults, intermediate in immatures, and absent in juveniles, suggesting that ontogeny influences species-specific microhabitat use. At night, all fishes, regardless of the species or age-class, congregated in shallow slow-flowing waters to rest on the river bottom. Our results suggest that placentation and superfetation may be hitherto unrecognized reproductive features that help to understand differences in ontogenetic and diurnal microhabitat preferences between sympatric live-bearing fish species.In Chapter 5, we examined the consequences of a trematode infestation (black spot disease) in shaping life-history and boldness in the placental live-bearing fish species P. retropinna from Costa Rica. We proposed that the intimate link the placenta forms between the mother and fetus poses a risk, because parasite infestation may affect fetal growth in two non-mutually exclusive ways: (i) directly, through infestation of the developing fetus by parasites that can cross the placental barrier; and (ii) indirectly, through the modification of maternal physiology or metabolism to such an extent that it interferes with fetal development. We showed that heavily parasitized females produced smaller and worse-conditioned offspring at birth, possibly because a costly immune response during pregnancy may limit the energy available to (i) nourish developing embryos or (ii) form a well-functioning placenta. However, the infestation rate did not affect an individual’s boldness in the field. Our findings show that in placental live-bearing fish parasite infestation leads to reduced embryo provisioning during pregnancy, resulting in a smaller offspring size and quality at birth potentially with negative implications for offspring fitness.In Chapter 6, we conducted a 7-week laboratory experiment to examine to what extent maternal food limitation during pregnancy affects offspring size and quality at birth, as well as growth and locomotor performance of offspring after birth in the placental live-bearing fish species Phalloptychus januarius. We showed that maternal food restriction resulted in a decrease in maternal wet mass throughout the experiment, leading to a reduced resource allocation to F1-offspring size and body fat, which can be compensated only in the long-term (i.e. when adult). This negatively affected the postnatal development of locomotor performance during feeding, and thus, body condition and presumably fitness after birth. This suggests that placentotrophy in poeciliids is likely a maladaptive strategy in fluctuating resource environments, because sudden reductions in maternal food availability during pregnancy result in smaller offspring with a lower locomotor performance during early life.In Chapter 7, I put the findings of this thesis into a wider scientific context. Because superfetation is commonly found in Poeciliidae and thought to co-evolve with the evolution of the placenta, I developed an R-package to simulate the potential advantages of having superfetation, as well as both, superfetation and placentation. The simulation shows that the co-evolution of placentation and superfetation might be favored by the additive effects of both traits on the reproductive burden of females during pregnancy. Moreover, I address the potential disadvantages of having a placenta in response to various adverse environmental conditions. Finally, I present an outlook on future research by addressing possible steps and challenges to deepen the knowledge on placental evolution

Limited mass‐independent individual variation in resting metabolic rate in a wild population of snow voles (Chionomys nivalis)

Resting metabolic rate (RMR) is a potentially important axis of physiological adaptation to the thermal environment. However, our understanding of the causes and consequences of individual variation in RMR in the wild is hampered by a lack of data, as well as analytical challenges. RMR measurements in the wild are generally characterized by large measurement errors and a strong dependency on mass. The latter is problematic when assessing the ability of RMR to evolve independently of mass. Mixed models provide a powerful and flexible tool to tackle these challenges, but they have rarely been used to estimate repeatability of mass‐independent RMR from field data. We used respirometry to obtain repeated measurements of RMR in a long‐term study population of snow voles (Chionomys nivalis) inhabiting an environment subject to large circadian and seasonal fluctuations in temperature. Using both uni‐ and bivariate mixed models, we quantify individual repeatability in RMR and decompose repeatability into mass‐dependent and mass‐independent components, while accounting for measurement error. RMR varies among individuals, that is, is repeatable (R = .46) and strongly co‐varies with BM. Indeed, much of the repeatability of RMR is attributable to individual variation in BM, and the repeatability of mass‐independent RMR is reduced by 41% to R = .27. These empirical results suggest that the evolutionary potential of RMR independent of mass may be severely constrained. This study illustrates how to leverage bivariate mixed models to model field data for metabolic traits, correct for measurement error and decompose the relative importance of mass‐dependent and mass‐independent physiological variation

Differences in ontogenetic and diurnal microhabitat selection by sympatric live-bearing fish species with different reproductive modes

A pregnancy imposes a heavy reproductive burden on females. Some live-bearing species have evolved reproductive adaptations to reduce this burden, which may influence their ability to utilize specific microhabitats. We investigate whether two such reproductive adaptations, placentation (embryo provisioning via a placenta) and superfetation (the ability to carry multiple broods at various developmental stages), influence microhabitat selection by five sympatric Costa Rican live-bearing fish species (family Poeciliidae). Theory predicts that placentation and superfetation should both reduce the reproductive burden of females during pregnancy, improve their body streamlining, and swimming performance, and consequently allow them to utilize ‘more performance-demanding’ microhabitats. Here we apply underwater visual fish surveys to test a key prediction of this hypothesis, which is that the presence of these two reproductive adaptations is correlated with the utilization of microhabitats in the river that are characterized by a higher-flow velocity. Consistent with our predictions, we observed significant interspecific differences in daytime microhabitat use: species that had both placentation and superfetation were found in deeper and faster-flowing parts of the river, species that lacked both adaptations were confined to shallow slow-flowing areas, and species with one adaptation (i.e. only superfetation) inhabited intermediate areas. This interspecific daytime microhabitat use was strongest in reproductive adults, intermediate in immatures, and absent in juveniles (the latter of which were all found in shallow low-velocity zones), suggesting that ontogeny influences species-specific microhabitat use. Finally, at night, all fishes, regardless of the species or age-class, congregated in shallow slow-flowing waters to rest (sleep) on the river bottom. Taken together, our results suggest that placentation and superfetation may be hitherto unrecognized reproductive features that help to understand differences in ontogenetic and diurnal microhabitat preferences between sympatric live-bearing fish species living in environments characterized by large flow variation

Parasite infestation influences life history but not boldness behavior in placental live-bearing fish

Parasites can negatively affect the reproductive success of hosts. Placental species may be particularly susceptible, because parasite-induced stress during pregnancy could potentially influence embryo development. Here, we examine the consequences of a trematode infestation (black spot disease, BSD) for fetal development and adult behavior in 19 natural populations of the placental live-bearing fish species Poeciliopsis retropinna (Poeciliidae) in Costa Rica. First, we observed substantial variation in parasite infestation among populations which correlated with a number of local environmental conditions (elevation, river width, depth, and flow velocity). Furthermore, we observed substantial variation in parasite infestation among females within populations associated with maternal age and size. We found that the infestation rate significantly influenced embryonic development, with more heavily parasitized females producing smaller and worse-conditioned offspring at birth, possibly, because a costly immune response during pregnancy limits, either directly or indirectly, nourishment to developing embryos. Finally, a behavioral experiment in the field showed that the infestation rate did not affect an individual’s boldness. Our study indicates that in placental live-bearing fish parasite infestation leads to reduced embryo provisioning during pregnancy, resulting in a smaller offspring size and quality at birth potentially with negative implications for offspring fitness.</p

Parasite infestation influences life-history but not boldness behavior in placental live-bearing fish

Parasites can negatively affect the reproductive success of hosts. Placental species may be particularly susceptible, because parasite-induced stress during pregnancy could potentially influence embryo development. Here we examine the consequences of a trematode infestation (black spot disease, BSD) for fetal development and adult behavior in 19 natural populations of the placental live-bearing fish species Poeciliopsis retropinna (Poeciliidae) in Costa Rica. First, we observed substantial variation in parasite infestation among populations which correlated with a number of local environmental conditions (elevation, river width, depth, and flow velocity). Furthermore, we observed substantial variation in parasite infestation among females within populations associated with maternal age and size. We found that the infestation rate significantly influenced embryonic development, with more heavily parasitized females producing smaller and worse-conditioned offspring at birth, possibly because a costly immune response during pregnancy limits, either directly or indirectly, nourishment to developing embryos. Finally, a behavioral experiment in the field showed that the infestation rate did not affect an individual’s boldness. Our study indicates that in placental live-bearing fish parasite infestation leads to reduced embryo provisioning during pregnancy, resulting in a smaller offspring size and quality at birth potentially with negative implications for offspring fitness

Female reproductive mode shapes allometric scaling of male traits in livebearing fishes (family Poeciliidae)

Reproductive mode is predicted to influence the form of sexual selection. The viviparity driven conflict hypothesis posits that a shift from lecithotrophic (yolk-nourished) to matrotrophic (mother-nourished or placental) viviparity drives a shift from pre-copulatory toward post-copulatory sexual selection. In lecithotrophic species, we predict that pre-copulatory sexual selection will manifest as males exhibiting a broad distribution of sizes, and small and large males exhibiting contrasting phenotypes (morphology and coloration); conversely, in matrotrophic species an emphasis on post-copulatory sexual selection will preclude these patterns. We test these predictions by gathering data on male size, morphology, and coloration for five sympatric Costa Rican poeciliid species that differ in reproductive mode (i.e. lecithotrophy vs matrotrophy). We find tentative support for these predictions of the viviparity driven conflict hypothesis, with some interesting caveats and subtleties. In particular, we find that the three lecithotrophic species tend to show a broader distribution of male sizes than matrotrophic species. Furthermore, large males of such species tend to exhibit proportionately large dorsal and caudal fins and short gonopodia relative to small males, while these patterns are expressed to a lesser extent in the two matrotrophic species. Finally, large males in some of the lecithotrophic species exhibit darker fins relative to small males, a pattern not evident in either matrotrophic species. One unexpected finding was that even in the matrotrophic species Poeciliopsis retropinna and Poeciliopsis paucimaculata, which lack courtship and dichromatic coloration, some morphological traits exhibit significant allometric relationships, suggesting that even in these species pre-copulatory sexual selection may be present and shaping size-specific male phenotypes in subtle ways

Female reproductive mode shapes allometric scaling of male traits in live-bearing fishes (family Poeciliidae)

Reproductive mode is predicted to influence the form of sexual selection. The viviparity-driven conflict hypothesis posits that a shift from lecithotrophic (yolk-nourished) to matrotrophic (mother-nourished or placental) viviparity drives a shift from precopulatory towards post-copulatory sexual selection. In lecithotrophic species, we predict that precopulatory sexual selection will manifest as males exhibiting a broad distribution of sizes, and small and large males exhibiting contrasting phenotypes (morphology and coloration); conversely, in matrotrophic species, an emphasis on post-copulatory sexual selection will preclude these patterns. We test these predictions by gathering data on male size, morphology and coloration for five sympatric Costa Rican poeciliid species that differ in reproductive mode (i.e. lecithotrophy vs. matrotrophy). We find tentative support for these predictions of the viviparity-driven conflict hypothesis, with some interesting caveats and subtleties. In particular, we find that the three lecithotrophic species tend to show a broader distribution of male sizes than matrotrophic species. Furthermore, large males of such species tend to exhibit proportionately large dorsal and caudal fins and short gonopodia relative to small males, while these patterns are expressed to a lesser extent in the two matrotrophic species. Finally, large males in some of the lecithotrophic species exhibit darker fins relative to small males, a pattern not evident in either matrotrophic species. One unexpected finding was that even in the matrotrophic species Poeciliopsis retropinna and Poeciliopsis paucimaculata, which lack courtship and dichromatic coloration, some morphological traits exhibit significant allometric relationships, suggesting that even in these species precopulatory sexual selection may be present and shaping size-specific male phenotypes in subtle ways

Limited mass-independent individual variation in resting metabolic rate in a wild population of snow voles (Chionomys nivalis)

Resting metabolic rate (RMR) is a potentially important axis of physiological adaptation to the thermal environment. However, our understanding of the causes and consequences of individual variation in RMR in the wild is hampered by a lack of data, as well as analytical challenges. RMR measurements in the wild are generally characterized by large measurement errors and a strong dependency on mass. The latter is problematic when assessing the ability of RMR to evolve independently of mass. Mixed models provide a powerful and flexible tool to tackle these challenges, but they have rarely been used to estimate repeatability of mass-independent RMR from field data. We used respirometry to obtain repeated measurements of RMR in a long-term study population of snow voles (Chionomys nivalis) inhabiting an environment subject to large circadian and seasonal fluctuations in temperature. Using both uni- and bivariate mixed models, we quantify individual repeatability in RMR and decompose repeatability into mass-dependent and mass-independent components, while accounting for measurement error. RMR varies among individuals, i.e. is repeatable (R=0.46), and strongly co-varies with BM. Indeed, much of the repeatability of RMR is attributable to individual variation in BM, and the repeatability of mass-independent RMR is reduced by 41% to R=0.27. These empirical results suggest that the evolutionary potential of RMR independent of mass may be severely constrained. This study illustrates how to leverage bivariate mixed models to model field data for metabolic traits, correct for measurement error, and decompose the relative importance of mass-dependent and mass-independent physiological variation