Fish Family Poeciliidae Research Articles

Repeated independent origins of the placenta reveal convergent and divergent organ evolution within a single fish family (Poeciliidae).

An outstanding question in biology is to what extent convergent evolution produces similar, but not necessarily identical, complex phenotypic solutions. The placenta is a complex organ that repeatedly evolved in the livebearing fish family Poeciliidae. Here, we apply comparative approaches to test whether evolution has produced similar or different placental phenotypes in the Poeciliidae and to what extent these phenotypes correlate with convergence at the molecular level. We show the existence of two placental phenotypes characterized by distinctly different anatomical adaptations (divergent evolution). Furthermore, each placental phenotype independently evolved multiple times across the family, providing evidence for repeated convergence. Moreover, our comparative genomic analysis revealed that the genomes of species with different placentas are evolving at a different pace. Last, we show that the two placental phenotypes correlate with two previously described contrasting life-history optima. Our results argue for high evolvability (both divergent and convergent) of the placenta within a group of closely related species in a single family.

Complete mitochondrial genome of a livebearing freshwater fish (Cyprinodontiformes: Poeciliidae): Poecilia parae

Members of the fish family Poeciliidae (livebearing ‘tooth-carps’) have historically been used as models in medical research, behavior ecology, and biological control. This group of primarily freshwater fishes is highly tolerant to environmental factors such as salinity and warm temperatures and includes some invasive species. Here, we present the mitochondrial genome of Poecilia parae. A representative of this species was obtained from Suriname. The complete mitochondrial genome was sequenced using Oxford Nanopore technology and is 16,559 bp long. The genome contains 13 protein-coding genes, two ribosomal RNAs (rRNAs), 22 transfer RNAs (tRNAs), and one control region (D-loop). Phylogenetic analysis yielded topologies similar to those previously published. The data generated here will be useful in future studies of comparative biology and those utilizing environmental DNA (eDNA).

Increased superfetation precedes the evolution of advanced degrees of placentotrophy in viviparous fishes of the family Poeciliidae.

The causes and consequences of the evolution of placentotrophy (post-fertilization nutrition of developing embryos of viviparous organisms by means of a maternal placenta) in non-mammalian vertebrates are still not fully understood. In particular, in the fish family Poeciliidae there is an evolutionary link between placentotrophy and superfetation (ability of females to simultaneously bear embryos at distinct developmental stages), with no conclusive evidence for which of these two traits facilitates the evolution of more advanced degrees of the other. Using a robust phylogenetic comparative method based on Ornstein-Uhlenbeck models of adaptive evolution and data from 36 poeciliid species, we detected a clear causality pattern. The evolution of extensive placentotrophy has been facilitated by the preceding evolution of more simultaneous broods. Therefore, placentas became increasingly complex as an adaptive response to evolutionary increases in the degree of superfetation. This finding represents a substantial contribution to our knowledge of the factors that have shaped placental evolution in poeciliid fishes.

Multiple paternity in superfetatious live-bearing fishes.

Superfetation, the ability to carry several overlapping broods at different developmental stages, has evolved independently multiple times within the live-bearing fish family Poeciliidae. Even though superfetation is widespread among poeciliids, its evolutionary advantages remain unclear. Theory predicts that superfetation should increase polyandry by increasing the probability that temporally overlapping broods are fertilized by different fathers. Here, we test this key prediction in two poeciliid species that each carry two temporally overlapping broods: Poeciliopsis retropinna and P. turrubarensis. We collected 25 females per species from freshwater streams in South-Eastern Costa Rica and assessed multiple paternity by genotyping all their embryos (420 embryos for P. retropinna; 788 embryos for P. turrubarensis) using existing and newly developed microsatellite markers. We observed a high frequency of unique sires in the simultaneous, temporally overlapping broods in P. retropinna (in 56% of the pregnant females) and P. turrubarensis (79%). We found that the mean number of sires within females was higher than the number of sires within the separate broods (2.92sires within mothers vs. 2.36 within separate broods in P. retropinna; and 3.40 vs 2.56 in P. turrubarensis). We further observed that there were significant differences in the proportion of offspring sired by each male in 42% of pregnant female P. retropinna and 65% of female P. turrubarensis; however, this significance applied to only 9% and 46% of the individual broods in P. retropinna and P. turrubarensis, respectively, suggesting that the unequal reproductive success of sires (i.e. reproductive skew) mostly originated from differences in paternal contribution between, rather than within broods. Together, these findings tentatively suggest that superfetation may promote polyandry and reproductive skew in live-bearing fishes.

Reproductive Mode and Conflict Shape the Evolution of Male Attributes and Rate of Speciation in the Fish Family Poeciliidae

Sexual conflict is caused by differences between the sexes in how fitness is maximized. These differences are shaped by the discrepancy in the investment in gametes, how mates are chosen and how embryos and young are provided for. Fish in the family Poeciliidae vary from completely provisioning eggs before they are fertilized to providing virtually all resources after fertilization via the functional equivalent of a mammalian placenta. This shift in when females provision their young relative to when an egg is fertilized is predicted to cause a fundamental change in when and how sexual conflict is manifested. If eggs are provisioned before fertilization, there should be strong selection for females to choose with whom they mate. Maternal provisioning after fertilization should promote a shift to post-copulatory mate choice. The evolution of maternal provisioning may in turn have cascading effects on the evolution of diverse features of the biology of these fish because of this shift in when mates are chosen. Here we summarize what these consequences are and show that the evolution of maternal provisioning is indeed associated with and appears to govern the evolution of male traits associated with sexual selection. The evolution of placentas and associated conflict does not cause accelerated speciation, contrary to predictions. Accelerated speciation rate is instead correlated with the evolution of male traits associated with sexual selection, which implies a more prominent role of pre-copulatory reproductive isolation in causing speciation in this family.

The Fish Family Poeciliidae as a Model to Study the Evolution and Diversification of Regenerative Capacity in Vertebrates

The capacity of regenerating a new structure after losing an old one is a major challenge in the animal kingdom. Fish have emerged as an interesting model to study regeneration due to their high and diverse regenerative capacity. To date, most efforts have focused on revealing the mechanisms underlying fin regeneration, but information on why and how this capacity evolves remains incomplete. Here, we propose the livebearing fish family Poeciliidae as a promising new model system to study the evolution of fin regeneration. First, we review the current state of knowledge on the evolution of regeneration in the animal kingdom, with a special emphasis on fish fins. Second, we summarize recent advances in our understanding of the mechanisms behind fin regeneration in fish. Third, we discuss potential evolutionary pressures that may modulate the regenerative capacity of fish fins and propose three new theories for how natural and sexual selection can lead to the evolution of fin regeneration: (1) signaling-driven fin regeneration, (2) predation-driven fin regeneration, and (3) matrotrophy-suppressed fin regeneration. Finally, we argue that fish from the family Poeciliidae are an excellent model system to test these theories, because they comprise of a large variety of species in a well-defined phylogenetic framework that inhabit very different environments and display remarkable variation in reproductive traits, allowing for comparative studies of fin regeneration among closely related species, among populations within species or among individuals within populations. This new model system has the potential to shed new light on the underlying genetic and molecular mechanisms driving the evolution and diversification of regeneration in vertebrates.

The evolution of the placenta in poeciliid fishes

How and why complex organs evolve is generally lost to history. The mammalian placenta, for example, was derived from a single common ancestor that lived over 100 million years ago.1-3 Therefore, the selective factors favoring this complex trait remain obscure. Species in the live-bearing fish family Poeciliidae have independently evolved placentas numerous times while retaining closely related non-placental sister species.4-7 This provides the raw material to test alternative hypotheses for the evolution of the placenta. We assemble an extensive species-level dataset on reproductive mode, life histories, and habitat, and then implement phylogenetic comparative methods to test adaptive hypotheses for the evolution of the placenta. We find no consistent family-wide associations between placentation and habitat. However, placental species exhibit significantly reduced reproductive allotment and have a higher likelihood of exhibiting superfetation (the ability to gestate multiple broods at different developmental stages). Both features potentially increase body streamlining and enhance locomotor performance during pregnancy, possibly providing selective advantage in performance-demanding environments such as those with high predation or fast water flow. Furthermore, we found significant interactions between body size and placentation for offspring size and fecundity. Relative to non-placental species, placentation is associated with higher fecundity and smaller offspring size in small-bodied species and lower fecundity and larger offspring size in large-bodied species. This pattern suggests that there may be two phenotypic adaptive peaks, corresponding to two selective optima, associated with placentation: one represented by small-bodied species that have fast life histories, and the second by large-bodied species with slow life histories.

High Degree of Multiple Paternity and Reproductive Skew in the Highly Fecund Live-Bearing Fish Poecilia gillii (Family Poeciliidae)

Multiple paternity is a common phenomenon within the live-bearing fish family Poeciliidae. There is a great variety in brood sizes of at least two orders-of-magnitude across the family. However, little is known about the ramifications of this remarkable variation for the incidence and degree of multiple paternity and reproductive skew. Mollies (subgenus Mollienesia, genus Poecilia) produce some of the largest broods in the family Poeciliidae, making them an excellent model to study the effects of intra-specific variation in brood size on patterns of multiple paternity. We collected samples of the live-bearing fish Poecilia gillii from 9 locations in Costa Rica. We measured body size of 159 adult females, of which 72 were pregnant. These samples had a mean brood size of 47.2 ± 3.0 embryos, ranging from 4 to 130 embryos. We genotyped 196 field-collected specimens with 5 microsatellite markers to obtain location-specific allele frequencies. In addition, we randomly selected 31 pregnant females, genotyped all their embryos (N = 1346) and calculated two different parameters of multiple paternity: i.e., the minimum number of sires per litter using an exclusion-based method (GERUD) and the estimated number of sires per litter using a maximum likelihood approach (COLONY). Based on these two approaches, multiple paternity was detected in 22 and 27 (out of the 31) females, respectively, with the minimum number of sires ranging from 1 to 4 (mean ± SE: 2.1 ± 0.16 sires per female) and the estimated number of fathers ranging from 1 to 9 (mean ± SE: 4.2 ± 0.35 sires per female). The number of fathers per brood was positively correlated with brood size, but not with female size. Next, we calculated the reproductive skew per brood using the estimated number of sires, and found that in 21 out of the 27 multiply sired broods sires did not contribute equally to the offspring. Skew was not correlated with either female size, brood size or the number of sires per brood. Finally, we discuss several biological mechanisms that may influence multiple paternity and reproductive skew in P. gillii as well as in the Poeciliidae in general.

The genome of the live-bearing fish Heterandria formosa implicates a role of conserved vertebrate genes in the evolution of placental fish

BackgroundThe evolution of complex organs is thought to occur via a stepwise process, each subsequent step increasing the organ’s complexity by a tiny amount. This evolutionary process can be studied by comparing closely related species that vary in the presence or absence of their organs. This is the case for the placenta in the live-bearing fish family Poeciliidae, as members of this family vary markedly in their ability to supply nutrients to their offspring via a placenta. Here, we investigate the genomic basis underlying this phenotypic variation in Heterandria formosa, a poeciliid fish with a highly complex placenta. We compare this genome to three published reference genomes of non-placental poeciliid fish to gain insight in which genes may have played a role in the evolution of the placenta in the Poeciliidae.ResultsWe sequenced the genome of H. formosa, providing the first whole genome sequence for a placental poeciliid. We looked for signatures of adaptive evolution by comparing its gene sequences to those of three non-placental live-bearing relatives. Using comparative evolutionary analyses, we found 17 genes that were positively selected exclusively in H. formosa, as well as five gene duplications exclusive to H. formosa. Eight of the genes evolving under positive selection in H. formosa have a placental function in mammals, most notably endometrial tissue remodelling or endometrial cell proliferation.ConclusionsOur results show that a substantial portion of positively selected genes have a function that correlates well with the morphological changes that form the placenta of H. formosa, compared to the corresponding tissue in non-placental poeciliids. These functions are mainly endometrial tissue remodelling and endometrial cell proliferation. Therefore, we hypothesize that natural selection acting on genes involved in these functions plays a key role in the evolution of the placenta in H. formosa.

Reproductive differences between three species of Brachyrhaphis livebearing fishes in Panamá

Both theory and the published literature support the importance of demographic selection for differences in life history traits between populations as well as between related species. Much attention in this area has been paid to species in the livebearing fish family Poeciliidae. I studied populations of three species of poeciliid fishes of the genus Brachyrhaphis (episcopi, roswithae, terrabensis) found from low to high elevation in western and central Panamá for reproductive life history phenotypes. To determine how reproductive life history phenotypic characters subject to both selection and environmental influence may vary between these species, field collections were made at the end of the wet and dry seasons over several years. Work with other poeciliid species suggested that these three stream species, found in different environments largely defined along an elevational gradient, may have evolved different responses in their reproductive timing and effort in response to differences in abiotic and biotic environmental factors. Differences were found between female wet and dry season reproductive output in all three species. Brachyrhaphis episcopi and B. roswithae showed similar responses to seasonal changes, with larger reproductive allotment (RA) and brood size but smaller embryo size in the wet season and a higher percentage of gravid females found in the wet season compared to the dry, 86% to 49% for B. episcopi and 71% to 45% for B. roswithae. Female B. terrabensis showed different responses to seasonal changes. RA, brood size and embryo size were all larger in the wet season than in the dry season. The percentage of gravid females among those of reproductive size was 37% in the wet season compared to 10% in the dry season. Patterns of male size varied between the three species, with more muted seasonal differences than was found with females of all three species. Brachyrhaphis terrabensis males showed a much wider size range, possibly indicative of two male reproductive strategies in the species. There is a gradient in several measures from lowland to highland species such as highland reproduction apparently stopping entirely in the dry season.

Why do placentas evolve? Evidence for a morphological advantage during pregnancy in live-bearing fish

A live-bearing reproductive strategy can induce large morphological changes in the mother during pregnancy. The evolution of the placenta in swimming animals involves a shift in the timing of maternal provisioning from pre-fertilization (females supply their eggs with sufficient yolk reserves prior to fertilization) to post-fertilization (females provide all nutrients via a placenta during the pregnancy). It has been hypothesised that this shift, associated with the evolution of the placenta, should confer a morphological advantage to the females leading to a more slender body shape during the early stages of pregnancy. We tested this hypothesis by quantifying three-dimensional shape and volume changes during pregnancy and in full-grown virgin controls of two species within the live-bearing fish family Poeciliidae: Poeciliopsis gracilis (non-placental) and Poeciliopsis turneri (placental). We show that P. turneri is more slender than P. gracilis at the beginning of the interbrood interval and in virgins, and that these differences diminish towards the end of pregnancy. This study provides the first evidence for an adaptive morphological advantage of the placenta in live-bearing fish. A similar morphological benefit could drive the evolution of placentas in other live-bearing (swimming) animal lineages.

Placental structures and their association with matrotrophy and superfetation in poeciliid fishes

AbstractBoth matrotrophy, the maternal provisioning of nutrients to developing embryos after fertilization, and superfetation, the simultaneous presence of two or more groups of embryos at different stages of development, occur at varying degrees among species of the fish family Poeciliidae. However, it is still unclear if these two reproductive modes depend on the presence of relatively complex placentas. We describe the ultrastructure of the maternal follicular placenta of 11 poeciliid fishes using electron microscopy. In addition, we quantified six ultrastructure characteristics that reflect the degree of complexity (number of vesicles, area of vesicles, number of microvilli, microvilli length, thickness of the maternal follicle and follicular area). Using phylogenetic comparative methods, we evaluated the relationship between degree of matrotrophy and placental characteristics. We also analysed the potential effect of the presence of superfetation on placental complexity. We found a positive relationship between the degree of matrotrophy and follicular area, number of microvilli and number and area of vesicles. Similarly, follicular area and number of microvilli were larger in species with superfetation than in those without superfetation. We conclude that high degrees of matrotrophy and superfetation are associated with placental characteristics that increase the efficiency of nutrient transfer between mother and embryos.

Predation effects on matrotrophy, superfetation and other life history traits in Phalloceros harpagos

AbstractThis study investigates the effect of a predation gradient on the female life history traits of the poeciliid live‐bearing fish Phalloceros harpagos from a tropical stream in Brazil. Females’ length at maturity, somatic dry mass, reproductive allotment and fecundity varied significantly among predation sites. Phalloceros harpagos from the high‐predation site showed smaller size at maturity and somatic dry mass, greater reproductive allotment and higher fecundity than the nonpredation site. In all sites, we observed superfetation: pregnant females with two broods at different developmental stages. The presence of superfetation was not observed before in other congeneric species, and it may represent an additional independent evolutionary origin of superfetation in the fish family Poeciliidae. Matrotrophy, the postfertilisation maternal provisioning of nutrients to developing embryos throughout gestation, was observed in all three sites, with values of the matrotrophy index above two. The population under high predation pressure showed the highest degree of matrotrophy (embryos quadruplicate their dry mass during development) and the greatest percentage of females with superfetation (44.4%). Some life history traits responded more strongly to predators’ presence and others to predator density. These results suggest that different predation regimes shape female life history traits, increasing fecundity in high‐predation sites. The results also suggest a link between the cost of reproduction and the evolution of matrotrophy and superfetation, potentially to reduce the risk of predation without reducing fecundity.

A Potential Cost of Long Genitalia in Male Guppies: the Effects of Current Speed on Reproductive Behaviour

AbstractIn the fish family Poeciliidae, male genitalia, the gonopodia, are remarkably diverse across species; however, we still do not have a good understanding of the evolutionary processes promoting this diversity. For one trait, gonopodium length, several studies support a role for sexual conflict in selection for longer gonopodia. However, genital elongation may come at a cost of reduced locomotor abilities (e.g. resulting from greater drag and resistance). In this study, we were interested in the potential role of natural selection on the evolution of gonopodium length in poeciliids. Specifically, we asked whether a greater genital length impedes male reproductive behaviours at higher flow rates in the Trinidadian guppy, Poecilia reticulata. Using a flow chamber, males were placed with females in low‐ and high‐flow regimes and reproductive behaviours were measured. We did not find evidence for a cost of bearing a longer gonopodium at high flow. However, males did alter their mating tactics in response to current flow. We discuss the implications of our findings, in the light of habitat selection, on the forms of selection operating on gonopodium length and the mating interactions between the sexes in poeciliids.

The evolution of the placenta drives a shift in sexual selection in livebearing fish.

The evolution of the placenta from a non-placental ancestor causes a shift of maternal investment from pre- to post-fertilization, creating a venue for parent-offspring conflicts during pregnancy. Theory predicts that the rise of these conflicts should drive a shift from a reliance on pre-copulatory female mate choice to polyandry in conjunction with post-zygotic mechanisms of sexual selection. This hypothesis has not yet been empirically tested. Here we apply comparative methods to test a key prediction of this hypothesis, which is that the evolution of placentation is associated with reduced pre-copulatory female mate choice. We exploit a unique quality of the livebearing fish family Poeciliidae: placentas have repeatedly evolved or been lost, creating diversity among closely related lineages in the presence or absence of placentation. We show that post-zygotic maternal provisioning by means of a placenta is associated with the absence of bright coloration, courtship behaviour and exaggerated ornamental display traits in males. Furthermore, we found that males of placental species have smaller bodies and longer genitalia, which facilitate sneak or coercive mating and, hence, circumvents female choice. Moreover, we demonstrate that post-zygotic maternal provisioning correlates with superfetation, a female reproductive adaptation that may result in polyandry through the formation of temporally overlapping, mixed-paternity litters. Our results suggest that the emergence of prenatal conflict during the evolution of the placenta correlates with a suite of phenotypic and behavioural male traits that is associated with a reduced reliance on pre-copulatory female mate choice.

Evolution of Placentas in the Fish Family Poeciliidae: An Empirical Study of Macroevolution

The placenta is a complex organ that mediates all physiological and endocrine interactions between mother and developing embryos. Placentas have evolved throughout the animal kingdom, but little is known about how or why the placenta evolved. We review hypotheses about the evolution of placentation and examine empirical evidence in support for these hypotheses by drawing on insights from the fish family Poeciliidae. The placenta evolved multiple times within this family, and there is a remarkable diversity in its form and function among closely related species, thus providing us with ideal material for studying its evolution. Current hypotheses fall into two categories: adaptive hypotheses, which propose that the placenta evolved as an adaptation to environmental pressures, and conflict hypotheses, which posit that the placenta evolved as a result of antagonistic coevolution. These hypotheses are not mutually exclusive. Each may have played a role at different stages of the evolutionary process.

INDEPENDENT EVOLUTION OF COMPLEX LIFE HISTORY ADAPTATIONS IN TWO FAMILIES OF FISHES, LIVE-BEARING HALFBEAKS (ZENARCHOPTERIDAE, BELONIFORMES) AND POECILIIDAE (CYPRINODONTIFORMES)

We have previously documented multiple, independent origins of placentas in the fish family Poeciliidae. Here we summarize similar analyses of fishes in the family Zenarchopteridae. This family includes three live-bearing genera. Earlier studies documented the presence of superfetation, or the ability to carry multiple litters of young in different stages of development in the same ovary, in some species in all three genera. There is also one earlier report of matrotrophy, or extensive postfertilization maternal provisioning, in two of these genera. We present detailed life-history data for approximately half of the species in all three genera and combine them with the best available phylogeny to make inferences about the pattern of life-history evolution within this family. Three species of Hemirhamphodon have superfetation but lack matrotrophy. Most species in Nomorhamphus and Dermogenys either lack superfetation and matrotrophy or have both superfetation and matrotrophy. Our phylogenetic analysis shows that matrotrophy may have evolved independently in each genus. In Dermogenys, matrotrophic species produce fewer, larger offspring than nonmatrotrophic species. In Nomorhamphus; matrotrophic species instead produce more and smaller offspring than lecithotrophic species. However, the matrotrophic species in both genera have significantly smaller masses of reproductive tissue relative to their body sizes. All aspects of these results are duplicated in the fish family Poeciliidae. We discuss the possible adaptive significance of matrotrophy in the light of these new results. The two families together present a remarkable opportunity to study the evolution of a complex trait because they contain multiple, independent origins of the trait that often include close relatives that vary in either the presence or absence of the matrotrophy or in the degree to which matrotrophy is developed. These are the raw materials that are required for either an analysis of the adaptive significance of the trait or for studies of the genetic mechanisms that underlie the evolution of the trait.

Life history of Xenodexia ctenolepis: implications for life history evolution in the family Poeciliidae

Xenodexia ctenolepis (Hubbs, 1950) is a uniquely asymmetrical species in the fish family Poeciliidae that is endemic to a remote region of Guatemala. In the present study, we describe its life history based on the dissection of 65 adult females from three different collections. We show that it is a livebearer, has superfetation, or the ability to carry multiple litters of young in different stages of development, and has matrotrophy, or placentation, which results in the dry mass of young at birth being three- to four-fold greater than the egg at fertilization. The size distribution of males is non-normal in a fashion that suggests a genetic polymorphism for age and size at maturity. Most phylogenies place Tomeurus gracilis as the sister taxon to the remaining members of the family Poeciliidae. Because Tomeurus is the sole egg-layer in the family, egg-laying is thought to represent the life history of the common ancestor. Because Xenodexia possesses three supposed derived traits (livebearing, superfetation and matrotrophy), this phylogenetic hypothesis suggests that Xenodexia has a highly derived life history with respect to other members of the family. By contrast, the most recent DNA-based phylogeny suggests Xenodexia is the sister taxon to the remainder of the family. If this proves to be true, it suggests that some or all of these life history traits may have been characteristic of the common ancestor to the family, then lost and re-evolved multiple times within the family.

Habitat predicts reproductive superfetation and body shape in the livebearing fish Poeciliopsis turrubarensis

Superfetation, the ability of females to simultaneously carry more than one brood at different developmental stages, is an unusual reproductive strategy that has independently evolved several times in the livebearing fish family Poeciliidae. Why this strategy has evolved remains uncertain. One hypothesis is that superfetation is a response to selective pressures that constrain the physical space within a female in which her offspring can develop. This hypothesis is reasonable, because superfetation should reduce the total volume needed to house developing embryos – that is, fewer large, fully developed embryos will be held by a superfetating female (with several broods at different developmental stages) than a non‐superfetating female (where all embryos reach a fully developed stage at the same time).In this study, we explore this ‘morphological constraint’ hypothesis of superfetation by examining the livebearing fish, Poeciliopsis turrubarensis. We found that populations vary markedly in degree of superfetation, with individuals carrying from two to four distinct broods across different geographic areas. These populations also occupy a range of habitat types: some populations occur in slow moving coastal rivers near the ocean, while other populations occur far inland in fast moving waters that drain steep mountain environments. In comparing populations from these two types of environments, we find a strong association between stream habitat type and the degree of superfetation within populations. Fish from inland populations have higher levels of superfetation than their coastal counterparts. In addition, geometric morphometric analysis revealed that inland populations are also more fusiform than fish from coastal locations. Combined, these two lines of evidence support the ‘morphological constraint’ hypothesis, and suggest that the life history strategy of superfetation could be driven by environmental pressures that favor a more streamlined phenotype.

Extrasynaptic localization of the glutamate transporter EAAT4 at Purkinje cell synapses

How and why complex organs evolve is generally lost to history. The mammalian placenta, for example, was derived from a single common ancestor that lived over 100 million years ago.1, 2, 3 Therefore, the selective factors favoring this complex trait remain obscure. Species in the live-bearing fish family Poeciliidae have independently evolved placentas numerous times while retaining closely related non-placental sister species.4, 5, 6, 7 This provides the raw material to test alternative hypotheses for the evolution of the placenta. We assemble an extensive species-level dataset on reproductive mode, life histories, and habitat, and then implement phylogenetic comparative methods to test adaptive hypotheses for the evolution of the placenta. We find no consistent family-wide associations between placentation and habitat. However, placental species exhibit significantly reduced reproductive allotment and have a higher likelihood of exhibiting superfetation (the ability to gestate multiple broods at different developmental stages). Both features potentially increase body streamlining and enhance locomotor performance during pregnancy, possibly providing selective advantage in performance-demanding environments such as those with high predation or fast water flow. Furthermore, we found significant interactions between body size and placentation for offspring size and fecundity. Relative to non-placental species, placentation is associated with higher fecundity and smaller offspring size in small-bodied species and lower fecundity and larger offspring size in large-bodied species. This pattern suggests that there may be two phenotypic adaptive peaks, corresponding to two selective optima, associated with placentation: one represented by small-bodied species that have fast life histories, and the second by large-bodied species with slow life histories.