Have superfetation and matrotrophy facilitated the evolution of larger offspring in poeciliid fishes?

Superfetation is the ability of females to simultaneously carry multiple broods of embryos, with each brood at a different developmental stage. Matrotrophy is the post‐fertilization maternal provisioning of nutrients to developing embryos throughout gestation. Several studies have demonstrated that, in viviparous fishes, superfetation and matrotrophy have evolved in a correlated way, such that species capable of bearing several simultaneous broods also exhibit advanced degrees of post‐fertilization provisioning. The adaptive value of the concurrent presence of both reproductive modes may be associated with the production of larger newborns, which in turn may result in enhanced offspring fitness. In this study, we tested two hypotheses: (1) species with superfetation and moderate or extensive matrotrophy give birth to larger offspring compared with species without superfetation or matrotrophy; (2) species with higher degrees of superfetation and matrotrophy (i.e. more simultaneous broods and increased amounts of post‐fertilization provisioning) give birth to larger offspring compared with species with relatively low degrees of superfetation and matrotrophy (i.e. fewer simultaneous broods and lesser amounts of post‐fertilization provisioning). Using different phylogenetic comparative methods and data on 44 species of viviparous fishes of the family Poeciliidae, we found a lack of association between offspring size and the combination of superfetation and matrotrophy. Therefore, the concurrent presence of superfetation and moderate or extensive matrotrophy has not facilitated the evolution of larger offspring. In fact, these traits have evolved differently. Superfetation and matrotrophy have accumulated gradual changes that largely can be explained by Brownian motion, whereas offspring size has evolved fluidly, experiencing changes that probably resulted from selective responses to the local conditions.     

VARIATION IN OFFSPRING SIZE WITH BIRTH ORDER IN PLACENTAL FISH: A ROLE FOR ASYMMETRIC SIBLING COMPETITION?

Asymmetric sibling competition arises when siblings with different competitive abilities share a limited resource. Such competition occurs in species with postnatal parental care and may also occur when mothers provision embryos between fertilization and birth (matrotrophy). We hypothesized that the combination of matrotrophy and the simultaneous provisioning of embryos in different stages of development (superfetation) leads to asymmetric competition between sibling embryos. Moreover, we expect the intensity of this competition to increase with the level of superfetation as high levels of superfetation result in greater temporal overlap between broods. This hypothesis predicts that offspring from early broods, which predominantly compete with less‐developed siblings, will be larger at birth than offspring from later broods, which experience competition from more and less‐developed siblings. Data on offspring size at birth from two populations of the highly matrotrophic fish, Heterandria formosa, and similar studies of poeciliid fish spanning a range of life histories are consistent with our hypothesis. Together these results suggest that sibling competition is a direct consequence of the evolution of matrotrophy and superfetation in poeciliid fish.     

Phylogenetic systematics of the viviparous halfbeak genera Dermogenys and Nomorhamphus (Teleostei:Hemiramphidae:Zenarchopterinae)

Among the 13 genera and over 100 species of halfbeaks, three genera - Dermogenys, Nomorhamphus and Hemirhamphodon – are internally fertilized and viviparous. These genera belong to a more inclusive clade, the Zenarchopterinae, that also includes Zenarchopterus , inferred to be internally fertilized and to lay fertilized eggs, and the monotypic Tondanichthys , also inferred to be internally fertilized. Whereas the Hemiramphidae are distributed worldwide, internally fertilized halfbeaks are restricted to Southeast Asia. Recent data from histological surveys of the gonads of both males and females as well as embryonic modifications associated with viviparity have been combined here with osteological characters in a phylogenetic analysis. Results indicate overwhelming support for a sister-group relationship between Hemirhamphodon and {Dermogenys + Nomorhamphus). Monophyly of the Dermogenys + Nomorhamphus clade is also well supported. These results confirm earlier suggestions that Dermogenys , as previously defined, is paraphyletic. Within the Dermogenys + Nomorhamphus clade, two monophyletic clades are supported:one comprises ten species including four new species (Dermogenys bruneiensis, Dermogenys robertsi, Dermogenys palawanensis and Dermogenys collettei) and the other comprises 13 species including three undescribed species (Nomorhamphus rossi, Nomorhamphus pinnimaculata and Nomorhamphus manifesta). Diagnoses for the species of Dermogenys and Nomorhamphus , as well as a natural classification for the included species, are presented.     

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.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 77–85.     

Molecular phylogenetic relationships and the coevolution of placentotrophy and superfetation in Poecilia (Poeciliidae: Cyprinodontiformes)

Members of Poeciliidae are used as model organisms for experimental studies on natural and sexual selection, and comparative studies of life-history evolution. The latter have demonstrated multiple origins of both superfetation and placentotrophy within Poeciliidae. Most recently, placentotrophy has been described in five species of Poecilia (Pamphorichthys), but only one of these (P.hasemani) shows evidence of superfetation. Here, we use a molecular phylogeny based on concatenated nuclear and mitochondrial gene sequences to test hypotheses of correlated evolution between superfetation and placentotrophy in Poecilia. Taxon sampling included all species in the subgenera Micropoecilia and Pamphorichthys for which the presence or absence of placentotrophy and superfetation have been determined, as well as representatives of all other Poecilia subgenera (Acanthophacelus, Limia, Mollienesia, Poecilia, Pseudolimia). Phylogenetic analyses were performed with maximum parsimony, maximum likelihood, and Bayesian methods; ancestral states for life-history characters were reconstructed with parsimony and SIMMAP; correlation analyses were performed with SIMMAP; and divergence times were estimated using a relaxed molecular clock. All subgenera in Poecilia were recovered as monophyletic. The basal split in Poecilia is between P. (Acanthophacelus)+P. (Micropoecilia) and the other five subgenera. In the latter clade, P. (Poecilia) is the sister-group to the remaining four subgenera. Within P. (Pamphorichthys), all analyses with the combined data set recovered P. (Pamphorichthys) araguaiensis as the sister taxon to P. (Pamphorichthys) hollandi, and P. (Pamphorichthys) scalpridens as the sister taxon to P. (Pamphorichthys) minor. P. (Pamphorichthys) hasemani was either the sister taxon to P. (Pamphorichthys) hollandi+P. (Pamphorichthys) minor (maximum likelihood, Bayesian) or the sister taxon to all other Pamphorichthys species (maximum parsimony). Ancestral state reconstructions suggest that placentotrophy and superfetation evolved on the same branch in P. (Micropoecilia), whereas placentotrophy evolved before superfetation in P. (Pamphorichthys). SIMMAP analyses indicate a statistically significant association between placentotrophy and superfetation. Within P. (Micropoecilia) both placentotrophy and superfetation evolved in ≤4 million years. Within P. (Pamphorichthys), superfetation evolved in ≤9 million years on the P. (Pamphorichthys) hasemani branch, and placentotrophy evolved in ≤10 million years in the common ancestor of this subgenus.     

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

Both 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.     

Convergent Evolution of Viviparity, Matrotrophy, and Specializations for Fetal Nutrition in Reptiles and Other Vertebrates

Quantitative analyses based upon the superimposition of phylogeneticand reproductive data have revealed that viviparity has originatedon at least 132 independent occasions among vertebrates, with98 of these origins having occurred among reptiles. The viviparouslineages have given rise to at least 24 matrotrophic clades,all but four of which are anamniotes. Traditional scenariosassume progressive, gradualistic evolution from oviparity tolecithotrophic viviparity to matrotrophic viviparity. However,mammalian evidence indicates that matrotrophy can precede theevolution of viviparity. Moreover, data on reptiles seem tobe consistent with a punctuated equilibrium model for viviparityand a saltatory model for incipient matrotrophy and placentation. Among the specializations for fetal nutrition, strong convergenceis evident at organismal, organological, and cytological levels.Examples include yolk sac placentation, trophotaeniae, and adaptationsfor embryonic cannibalism. Certain lizards of the genera Mabuyaand Chalcides have converged strongly on eutherian mammals withrespect to morphology of the chorioallantoic placenta. Placentalspecializations that have evolved independently in some eutheriansand matrotrophic lizards include placentomes, giant binucleatecells, deciduate maternal tissue, and chorionic areolae.     

Resource allocation in offspring provisioning: an evaluation of the conditions favoring the evolution of matrotrophy

We used analytic and simulation models to determine the ecological conditions favoring evolution of a matrotrophic fish from a lecithotrophic ancestor given a complex set of trade-offs. Matrotrophy is the nourishment of viviparous embryos by resources provided between fertilization and parturition, while lecithotrophy describes embryo nourishment provided before fertilization. In fishes and reptiles, embryo nourishment encompasses a continuum from solely lecithotrophic to primarily matrotrophic. Matrotrophy has evolved independently from lecithotrophic ancestors many times in many groups. We assumed matrotrophy increased the number of offspring a viviparous female could gestate and evaluated conditions of food availability favoring lecithotrophy or matrotrophy. The matrotrophic strategy was superior when food resources exceeded demand during gestation but at a risk of overproduction and reproductive failure if food intake was limited. Matrotrophic females were leaner during gestation than lecithotrophic females, yielding shorter life spans. Our models suggest that matrotrophic embryo nourishment evolved in environments with high food availability, consistently exceeding energy requirements for maintaining relatively large broods. Embryo abortion with some resorption of invested energy is a necessary preadaptation to the evolution of matrotrophy. Future work should explore trade-offs of age-specific mortality and reproductive output for females maintaining different levels of fat storage during gestation.     

DO EMBRYOS INFLUENCE MATERNAL INVESTMENT? EVALUATING MATERNAL‐FETAL COADAPTATION AND THE POTENTIAL FOR PARENT‐OFFSPRING CONFLICT IN A PLACENTAL FISH

The evolution of matrotrophy introduces the potential for genomic conflicts between mothers and embryos. These conflicts are hypothesized to accelerate the evolution of reproductive isolation and to influence the evolution of life-history traits, reproductive structures, and genomic imprinting. These hypotheses assume offspring can influence the amount of maternal investment they receive and that there is a trade-off between maternal investment into individual offspring and maternal survival or fecundity. We used field data and laboratory crosses to test whether these assumptions are met in the matrotrophic poeciliid fish Heterandria formosa . Comparisons of life histories between two natural populations demonstrated a trade-off between the level of maternal investment into individual embryos and maternal fecundity. Laboratory crosses between individuals from these populations revealed that offspring genotype exerts an influence on the level of maternal investment and affects maternal fecundity through higher rates of embryo abortion and lower numbers of full-term offspring. Our results show that the prerequisites for parent–offspring conflict to be a potent evolutionary force in poeciliid fish are present in H. formosa. However, determining whether this conflict has shaped maternal investment in nature will require disentangling any effects of conflict from those of several ecological factors that are themselves correlated with the expected intensity of conflict.     

Matrotrophy and placentation in invertebrates: a new paradigm

Matrotrophy, the continuous extra‐vitelline supply of nutrients from the parent to the progeny during gestation, is one of the masterpieces of nature, contributing to offspring fitness and often correlated with evolutionary diversification. The most elaborate form of matrotrophy—placentotrophy—is well known for its broad occurrence among vertebrates, but the comparative distribution and structural diversity of matrotrophic expression among invertebrates is wanting. In the first comprehensive analysis of matrotrophy across the animal kingdom, we report that regardless of the degree of expression, it is established or inferred in at least 21 of 34 animal phyla, significantly exceeding previous accounts and changing the old paradigm that these phenomena are infrequent among invertebrates. In 10 phyla, matrotrophy is represented by only one or a few species, whereas in 11 it is either not uncommon or widespread and even pervasive. Among invertebrate phyla, Platyhelminthes, Arthropoda and Bryozoa dominate, with 162, 83 and 53 partly or wholly matrotrophic families, respectively. In comparison, Chordata has more than 220 families that include or consist entirely of matrotrophic species. We analysed the distribution of reproductive patterns among and within invertebrate phyla using recently published molecular phylogenies: matrotrophy has seemingly evolved at least 140 times in all major superclades: Parazoa and Eumetazoa, Radiata and Bilateria, Protostomia and Deuterostomia, Lophotrochozoa and Ecdysozoa. In Cycliophora and some Digenea, it may have evolved twice in the same life cycle. The provisioning of developing young is associated with almost all known types of incubation chambers, with matrotrophic viviparity more widespread (20 phyla) than brooding (10 phyla). In nine phyla, both matrotrophic incubation types are present. Matrotrophy is expressed in five nutritive modes, of which histotrophy and placentotrophy are most prevalent. Oophagy, embryophagy and histophagy are rarer, plausibly evolving through heterochronous development of the embryonic mouthparts and digestive system. During gestation, matrotrophic modes can shift, intergrade, and be performed simultaneously. Invertebrate matrotrophic adaptations are less complex structurally than in chordates, but they are more diverse, being formed either by a parent, embryo, or both. In a broad and still preliminary sense, there are indications of trends or grades of evolutionarily increasing complexity of nutritive structures: formation of (i) local zones of enhanced nutritional transport (placental analogues), including specialized parent–offspring cell complexes and various appendages increasing the entire secreting and absorbing surfaces as well as the contact surface between embryo and parent, (ii) compartmentalization of the common incubatory space into more compact and ‘isolated’ chambers with presumably more effective nutritional relationships, and (iii) internal secretory (‘milk’) glands. Some placental analogues in onychophorans and arthropods mimic the simplest placental variants in vertebrates, comprising striking examples of convergent evolution acting at all levels—positional, structural and physiological.     

Effects of Maternal Basking and Food Quantity during Gestation Provide Evidence for the Selective Advantage of Matrotrophy in a Viviparous Lizard

The evolution of matrotrophy (i.e., direct supply of nutrients by the mother during gestation) may be associated with high maternal energy availability during gestation. However, we lack knowledge about the selective advantages of matrotrophic viviparity (live-bearing) in reptiles. In reptiles, the interaction between body temperature and food intake affect maternal net energy gain. In the present study, we examined the effects of basking and food availability (2 by 2 factorial design) during gestation on offspring phenotype in a matrotrophic viviparous lizard (Pseudemoia entrecasteauxii). Subsequently, we investigated if the maternal effects were context-dependent using offspring growth rate as an indicator of the adaptive significance of matrotrophy. Offspring were exposed either to the same thermal conditions as their mothers experienced or to thermal conditions different from those experienced by their mothers. We provide the first evidence that an interaction between maternal thermal and maternal food conditions during gestation strongly affects offspring phenotype, including date of birth, body size and performance ability, which affect offspring fitness. Offspring growth rate was dependent on offspring thermal conditions, but was not influenced by maternal effects or offspring sex. Matrotrophic viviparity provided gravid females with the means to enhance offspring fitness through greater energetic input to offspring when conditions allowed it (i.e., extended basking opportunity with high food availability). Therefore, we suggest that selective advantages of matrotrophic viviparity in P. entrecasteauxii may be associated with high maternal energy availability during gestation.     

Maternal Effects on Offspring Quality in Poeciliid Fishes

SYNOPSIS. We evaluated the effects of maternal environment onoffspring size and composition in three species of poeciliidfishes. We chose food availability as the environmental factorfor study. Mature females were assigned to either high or lowfood for an interval of time, then randomly reassigned to highor low food, with the restriction that there be equal numbersin each of four treatments: high-high, high-low, lowhigh, andlow-low food availability. The three species chosen for studydiffer in the pattern of maternal provisioning. Poecilia reticulataand Priapichthys festae mothers provide all resources necessaryfor development as yolk, prior to fertilization. In contrast,Heterandria formosa mothers continue to provision the youngthroughout development. These species also differ in whetheror not they have superfetation, or the ability to carry multiplebroods of young in different stages of development. P. reticulatadoes not have superfetation while the other two species do.We were interested in whether the pattern of maternal provisioningor superfetation influenced the maternal effect. The two lecithotrophicspecies responded to low food by producing larger young withgreater fat reserves. H. formosa, the matrotrophic species,responded to low food by producing smaller young. We proposethat the production of large young in the face of low food availabilitymight represent adaptive plasticity; matrotrophy might representa constraint that prevents such an adaptive response. Superfetationhad no impact on this maternal effect.     

Superfetation increases total fecundity in a viviparous fish regardless of the ecological context

Superfetation is the ability of females to simultaneously carry multiple broods of embryos at different developmental stages. This is an uncommon reproductive strategy that has evolved independently several times in viviparous fishes. The ecological conditions that favor higher degrees of superfetation (the presence of more simultaneous broods) still remain unclear. In this study we tested hypotheses about the potential effects of three particular ecological factors (water flow velocity, population density, and adult mortality) on superfetation. We used data on six populations of one fish species from the family Poeciliidae (Poeciliopsis baenschi) and a multimodel inference framework to test these hypotheses. We found no clear associations between the degree of superfetation and these ecological factors. Instead, we found a positive relationship between the total number of embryos carried by females and superfetation. Females increased their total fecundity as they overlapped more broods and this pattern was independent of the particular ecological conditions. Thus, in P. baenschi superfetation may facilitate a greater reproductive output. In addition, this positive relationship between total number of embryos and superfetation was stronger in small- and medium-sized females, whereas large females produced few or no simultaneous broods regardless of their total fecundity. The observed lack of association between superfetation and ecological variables is noteworthy because previous studies on other congeneric species have found that superfetation may vary as a function of water flow velocity or food availability. Our results indicate that the effect of particular selective factors on the degree of superfetation may differ among closely related species.     

Matrotrophy in the cave molly: an unexpected provisioning strategy in an extreme environment

Maternal provisioning of animal embryos may be entirely through yolk deposited in the unfertilized egg (lecithotrophy) or may include post-fertilization nutrient transfer (matrotrophy) in varying degrees. Current theory suggests that the extent of post-fertilization provisioning is resource-dependent, with higher levels of matrotrophy being advantageous in more productive environments. In this study, we investigated post-fertilization embryo provisioning in a livebearing fish, Poecilia mexicana, from two different habitats (a toxic cave and a non-toxic surface habitat) that impose different energetic demands and therefore differ in resources available for reproduction. We predicted that fish in the benign habitat would be more matrotrophic than those from the toxic cave. We used two different techniques for this assay: (1) the matrotrophy-index analysis (MI) for field-collected fish and (2) both MI and radio-tracer assay for laboratory-reared females. According to the interpretation of the matrotrophy index, both populations are purely lecithotrophic, while the radio-tracer assay found females from both populations to actively transfer nutrients to developing embryos at approximately the same rate. Our results suggest that P. mexicana, which was traditionally classified as lecithotrophic, is capable of incipient matrotrophy, and that matrotrophy can contribute to embryo provisioning even in populations from resource-limited environments. Furthermore, the analysis of laboratory-reared animals provides evidence for a genetic component to the large offspring size in cave mollies, which had so far only been described from the field. Specifically, our results suggest matrotrophy occurs in species interpreted as lecithotrophic using the MI approach. Hence, to avoid misclassification, both techniques should ideally be employed in concert, rather than individually. Finally, our results provide further insights into the possible evolutionary pathway from lecithotrophic oviparity to matrotrophic viviparity.     

Evidence of multiple paternity in the bluntnose klipfish, <Emphasis Type="Italic">Clinus cottoides</Emphasis> (Blennioidei: Clinidae: Clinini)

Clinids of the tribe Clinini are viviparous fishes occurring in the temperate waters of southern Africa. Females of the genus Clinus exhibit reproductive traits suggesting multiple paternity. These traits include prolonged gestation periods, matrotrophy and superfetation. We tested the hypothesis that broods of the species C. cottoides are sired by multiple males with the use of microsatellites. We genotyped three broods from known mothers and analysed the relationships within each brood using the software program COLONY, we also used allele counting to find evidence of multiple paternity. Our results revealed that multiple paternity occurred in all three broods analysed; two broods likely had two sires and one brood three sires. One male appear to have fathered offspring with separate females. Our study represents the first molecular analysis of parentage in C. cottoides.     

Superfetation in the viviparous fish Heterandria formosa (Poeciliidae)

Heterandria formosa is a viviparous poeciliid native of the southeastern of United States of America. H. formosa exhibits unique reproductive features as: (a) production of extremely small eggs with scarce quantity of yolk (microlecithal eggs), (b) consequently, a high level of matrotrophy and development of a complex follicular placenta, (c) ovarian sperm storage that allows the continuous fertilization of oocytes and production of offspring and (d) development of high degree of superfetation. The degree of superfetation refers to the number of broods in different simultaneous stages of gestation. Morphological evidence of the degree of superfetation in H. formosa has not been documented. Therefore, and because of the general interest in the complex process of superfetation, the goal of this study is to morphologically define the degree of superfetation of H. formosa through two procedures: (a) histological analysis of entire ovaries in gestation and (b) dissection of visible embryos and the histological analysis of the remaining ovarian tissue. Results indicate that H. formosa can gestate up to seven broods at the same time.     

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.     

Parallel Genomic Changes Drive Repeated Evolution of Placentas in Live-Bearing Fish

The evolutionary origin of complex organs challenges empirical study because most organs evolved hundreds of millions of years ago. The placenta of live-bearing fish in the family Poeciliidae represents a unique opportunity to study the evolutionary origin of complex organs, because in this family a placenta evolved at least nine times independently. It is currently unknown whether this repeated evolution is accompanied by similar, repeated, genomic changes in placental species. Here, we compare whole genomes of 26 poeciliid species representing six out of nine independent origins of placentation. Evolutionary rate analysis revealed that the evolution of the placenta coincides with convergent shifts in the evolutionary rate of 78 protein-coding genes, mainly observed in transporter- and vesicle-located genes. Furthermore, differences in sequence conservation showed that placental evolution coincided with similar changes in 76 noncoding regulatory elements, occurring primarily around genes that regulate development. The unexpected high occurrence of GATA simple repeats in the regulatory elements suggests an important function for GATA repeats in developmental gene regulation. The distinction in molecular evolution observed, with protein-coding parallel changes more often found in metabolic and structural pathways, compared with regulatory change more frequently found in developmental pathways, offers a compelling model for complex trait evolution in general: changing the regulation of otherwise highly conserved developmental genes may allow for the evolution of complex traits.     

Colonisation of toxic environments drives predictable life‐history evolution in livebearing fishes (Poeciliidae)

New World livebearing fishes (family Poeciliidae) have repeatedly colonised toxic, hydrogen sulphide‐rich waters across their natural distribution. Physiological considerations and life‐history theory predict that these adverse conditions should favour the evolution of larger offspring. Here, we examined nine poeciliid species that independently colonised toxic environments, and show that these fishes have indeed repeatedly evolved much larger offspring size at birth in sulphidic waters, thus uncovering a widespread pattern of predictable evolution. However, a second pattern, only indirectly predicted by theory, proved additionally common: a reduction in the number of offspring carried per clutch (i.e. lower fecundity). Our analyses reveal that this secondary pattern represents a mere consequence of a classic life‐history trade‐off combined with strong selection on offspring size alone. With such strong natural selection in extreme environments, extremophile organisms may commonly exhibit multivariate phenotypic shifts even though not all diverging traits necessarily represent adaptations to the extreme conditions.