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.     

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.     

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.     

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.     

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.     

Parent-offspring conflict in the evolution of vertebrate reproductive mode

We propose and evaluate the hypothesis that parent-offspring conflict over the degree of maternal investment has been one of the main selective factors in the evolution of vertebrate reproductive mode. This hypothesis is supported by data showing that the assumptions of parent-offspring conflict theory are met for relevant taxa; the high number of independent origins of viviparity, matrotrophy (direct maternal-fetal nutrient transfer), and hemochorial placentation (direct fetal access to the maternal bloodstream); the extreme diversity in physiological and morphological aspects of viviparity and placentation, which usually cannot be ascribed adaptive significance in terms of ecological factors; and divergent and convergent patterns in the diversification of placental structure, function, and developmental genetics. This hypothesis is also supported by data demonstrating that embryos and fetuses actively manipulate their interaction with the mother, thereby garnishing increased maternal resources. Our results indicate that selection may favor adaptations of the mother, the fetus, or both in traits related to reproductive mode and that integration of physiological and morphological data with evolutionary ecological data will be required to understand the adaptive significance of interspecific variation in viviparity, matrotrophy, and placentation.     

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.     

Follicular placenta of the viviparous fish,Heterandria formosa: II. Ultrastructure and development of the follicular epithelium

Embryos of the viviparous poeciliid fish, Heterandria formosa, develop to term in the ovarian follicle where they undergo a 3,900% increase in embryonic dry weight. Maternal-embryonic nutrient transfer occurs across a follicular placenta that is formed by close apposition of the embryonic surface (i.e., the entire body surface during early gestation and the pericardial amnionserosa during mid-late gestation) to the follicular epithelium. To complement our recent study of the embryonic component of the follicular placenta, we now describe the development and fine structure of the maternal component of the follicular placenta. Transmission electron microscopy reveals that the ultrastructure of the egg envelope and the follicular epithelium that invests vitellogenic oocytes is typical of that described for teleosts. The egg envelope is a dense matrix, penetrated by microvilli of the oocyte. The follicular epithelium consists of a single layer of cuboidal cells that lack apical microvilli, basal surface specializations, and junctional complexes. Follicle cells investing the youngest embryonic stage examined (Tavolga's and Rugh's stage 5–7 for Xiphophorus maculatus) also lack apical microvilli and basal specializations, but possess junctional complexes. In contrast, follicle cells that invest embryos at stage 10 and later display ultrastructural features characteristic of transporting epithelial cells. Apical microvilli and surface invaginations are present. The basal surface is extensively folded. Apical and basal coated pits are present. The cytoplasm contains a rough endoplasmic reticulum, Golgi complexes, and dense staining vesicles that appear to be lysosomes. The presence of numerous apically located electron-lucent vesicles that appear to be derived from the apical surface further suggests that these follicle cells may absorb and process follicular fluid. The egg envelope, which remains intact throughout gestation and lacks perforations, becomes progressively thinner and less dense as gestation proceeds. We postulate that these ultrastructural features, which are not present in the follicles of the lecithotrophic poeciliid, Poecilia reticulata, are specializations for maternal-embryonic nutrient transfer and that the egg envelope, follicular epithelium, and underlying capillary network form the maternal component of the follicular placenta. © 1994 Wiley-Liss, Inc.     

The follicular placenta of the viviparous fish,Heterandria formosa. I. Ultrastructure and development of the embryonic absorptive surface

Embryos of the poeciliid Heterandria formosa develop to term in the ovarian follicle in which they establish a placental association with the follicle wall (follicular placenta) and undergo a 3,900% increase in embryonic dry weight. This study does not confirm the belief that the embryonic component of the follicular placenta is formed only by the surfaces of the pericardial and yolk sacs; early in development the entire embryonic surface functions in absorption. The pericardial sac expands to form a hood-like structure that covers the head of the embryo and together with the yolk sac is extensively vascularized by a portal plexus derived from the vitelline circulation. The hood-like pericardial sac is considered to be a pericardial amnion-serosa. Scanning and transmission electron microscopy reveal that during the early and middle phases of development (Tavolga's stages 10–18 for Xiphophorus maculatus) the entire embryo is covered by a bilaminar epithelium whose apical surface is characterized by numerous, elongate microvilli and coated pits and vesicles. Electron-lucent vesicles in the apical cytoplasm appear to be endosomes while a heterogeneous group of dense-staining vesicles display many features characteristic of lysosomes. As in the larvae of other teleosts, cells resembling chloride cells are also present in the surface epithelium. Endothelial cells of the portal plexus lie directly beneath the surface epithelium of the pericardial and yolk sacs and possess numerous transcytotic vesicles. The microvillous surface epithelium becomes restricted to the pericardial and yolk sacs late in development when elsewhere on the embryo the non-absorptive epidermis differentiates. We postulate that before the definitive epidermis differentiates, the entire embryonic surface constitutes the embryonic component of the follicular placenta. The absorptive surface epithelium appears to be the principle embryonic adaptation for maternal-embryonic nutrient uptake in H. formosa, suggesting that a change in the normal differentiation of the surface epithelium was of primary importance to the acquisition of matrotrophy in this species. In other species of viviparous poeciliid fishes in which there is little or no transfer of maternal nutrients, the embryonic surface epithelium is of the non-absorptive type.     

An examination of the variation in maternal placentae across the genus Poeciliopsis (Poeciliidae)

Placentae show considerable diversity in a number of nonmammalian, viviparous organisms, including amphibians, reptilian sauropsids, teleost fish, and chondrichthyes. However, the evolutionary processes driving the evolution of placenta are still debated. In teleost fishes, the genus Poeciliopsis (Poeciliidae) offers a rare opportunity for studying placental evolution: extensive placentation has evolved three independent times within the last 750,000 years and there is substantial interspecific variation in the degree of embryonic, maternal nutrient provisioning and development of the placenta. In poeciliids, the placenta is composed of a hypertrophied maternal follicular epithelium apposed to a highly vascularized embryonic pericardial sac. To better understand placental evolution, we have undertaken a comprehensive comparative study of the maternal follicle in eight closely related Poeciliopsis species that span the range in postfertilization, embryonic, maternal nutrient provisioning (from lecithotrophs, to moderate matrotrophs, to extensive matrotrophs). Using light and scanning electron microscopy, we found that the species that provide extensive postfertilization maternal nutrient provisioning (extensive matrotrophs) have thicker follicles and more extensive folding of the follicular epithelium compared to the lecithotrophs and moderate matrotrophs. Follicle sections and histology revealed that epithelial folds of the extensive matrotrophs are comprised primarily of cuboidal and columnar cells and are richly supplied with capillaries. Among the extensive matrotrophs, enhancements of follicle traits corresponded with increases in the level of maternal nutrient provisioning. Hypertrophied maternal follicles with richly vascularized folds can serve to increase the surface area and, thus, facilitate the transfer of substances between the mother and developing embryo. Finally, we found egg envelopes in the lecithotrophs and moderate matrotrophs, but not in the extensive matrotrophs. Morphological studies, like this one, can provide a better understanding of the natural variation in the structure and functioning of maternal and offspring traits associated with matrotrophy and, thus, insights into the processes driving placental evolution. J. Morphol. 276:707–720, 2015. © 2015 Wiley Periodicals, Inc.     

Morphological structures for potential sperm storage in poeciliid fishes. Does superfetation matter?

Sperm storage within the female reproductive tract has been reported as a reproductive strategy in several species of vertebrates and invertebrates. However, the morphological structures that allow for sperm to be stored and kept viable for long periods are relatively unknown in osteichthyes. We use histological and stereological tools to identify and quantify sperm storage structures (spermathecae) in 12 species of viviparous Poeciliidae. We found spermathecae in nine species, six of which exhibit superfetation (the ability of females to simultaneously carry within the ovary two or more broods of embryos at different stages of development). These spermathecae are folds of ovarian tissue that close around spermatozoa. We compared the number and size (volume) of spermathecae between species with and without superfetation. Species that exhibit superfetation had a significantly higher number of spermathecae than species that do not exhibit this reproductive strategy. In addition, we found that the mean volume of spermathecae and total volume of spermathecae present in the ovary are marginally higher in species with superfetation. Our results contribute to the understanding of the morphological structures that allow for sperm storage in viviparous osteichthyes and suggest a positive relationship between superfetation and the capacity of females to store sperm.     

Structure and function of placental exchange surfaces in goodeid fishes (Teleostei: Atheriniformes)

The species of the family Goodeidae have evolved reproductive strategies involving intraovarian gestation, early evacuation of nearly yolk‐exhausted embryos from the ovigerous tissue into the ovarian cavity, placental matrotrophy during intraluminal gestation, and the birth of highly developed fry. The inner ovarian lining becomes hypervascularized during gestational periods and functions as the maternal component of the placental association. Embryotrophic liquid is secreted by the inner ovarian epithelium into the ovarian cavity. Comparative electrophoretic analyses of embryotrophe and maternal blood serum provide evidence for the transfer of maternal serum proteins into the embryotrophe. Trophotaeniae, proctodaeal processes of the embryos, provide a surface for nutrient absorption. Endocytic activity was demonstrated by ingestion of unspecific tracer proteins in various species. Moreover, the trophotaenial absorptive cells (TACs) in Ameca splendens ingest various proteins or random copolymers conjugated to colloidal gold as well as radioiodinated proteins in a way that satisfies the criteria of receptor‐mediated endocytosis. Several aminopeptidases (APs) on the surface of TACs were identified as protein binding sites as evidenced by inhibition of binding and uptake of marker proteins in the presence of AP substrates or AP inhibitors. Morphological adaptations of the embryonic circulatory system pertaining to nutrient and gas exchange were characterized. The embryonic epidermis comprises two layers of squamous cells closely underlain by a dense capillary net. Efficient gas exchange is facilitated by a thin embryotrophe‐blood barrier of both the embryonic skin and the intraovarian lining. J. Morphol. 276:991–1003, 2015. © 2014 Wiley Periodicals, Inc.     

Oocyte size and structure in relation to blood plasma steroid hormones in individually monitored, spawning Atlantic cod

A series of seasonal blood and ovarian tissue samples were taken from five female Atlantic cod Gadus morhua at different times between various batches of eggs and subsequently examined for oocyte size, plasma steroid hormones and ultrastructure of the cortex oocyte cytoplasm and follicle layer. This detailed protocol demonstrated that the spawning cod ovary is vitellogenically very active. Individual oocytes were able to develop at different rates, and at least two cohorts of oocytes with a different developmental status were present simultaneously. The concentration of estradiol-17β varied between batches and decreased over the season. The levels of 17,20β-P and 11-deoxycortisol were generally low. Oocytes of an advanced developing cohort showed numerous coated vesicles and closely apposed oocytic and follicular microvilli located in the chorionic pores. The number of oocytic microvilli was estimated at about 1–8 million cell⁻¹, which increased the oocyte surface area by a factor of 12. Furthermore, the oocytic microvilli were found to stretch during final maturation. This stage-specific mobility of microvilli is discussed in relation to further incorporation of yolk and the relevant actin-based cytoskeleton observed for other classes of animals.     

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.     

Ovarian follicle ultrastructure in the teleost Synbranchus marmoratus (Bloch, 1795), with special reference to the vitelline envelope development

Synbranchus marmoratus is a protogynous diandric teleost fish widely distributed throughout South America. The aim of this work was to study the ultrastructure of the vitelline envelope and the relationship among oocyte and their follicular cells during oogenesis. During perinucleolar stage, the oocyte and the follicular cells form microvillar processes that project into the perivitelline space. The oocyte secretes a dense and amorphous material, which appears as the first evidence of the vitelline envelope (VE) development. The VE passes from a double to a multilayered structure during oocyte growth. In mature oocytes, the VE reach a mean thickness of 11 microm, having up to 30 layers. Oocyte microvilli are thinner than the follicular ones and were seen in contact with the follicular plasmalema, however we could not find any contact between the follicular microvilli and the oolemma. Before ovulation, microvillar processes retract and the pore canals seem to collapse. An outer electron dense layer occludes the superficial pore and forms a continuous layer. No jelly or adhesive coatings were seen at least in ovulated eggs sampled from ovarian lumen. Follicular cell and oocyte cytological characteristics do not differ from those described in other teleosts species.     

Placentation in garter snakes. II. Transmission EM of the chorioallantoic placenta of Thamnophis radix and T. sirtalis

Transmission electron microscopy was used to examine the ultrastructure of the allantoplacenta of garter snakes during the last half of gestation. This placenta occupies the dorsal hemisphere of the egg and is formed through apposition of the chorioallantois to the inner lining of the uterus. The uterine epithelium consists of flattened cells with short, irregular microvilli and others that bear cilia. The lamina propria is vascularized and its capillaries lie at the base of the uterine epithelial cells. The chorionic epithelium consists of a bilayer of squamous cells that are particularly thin superficial to the allantoic capillaries. Neither the chorionic epithelium nor the uterine epithelium undergoes erosion during development. Although a thin remnant of the shell membrane intervenes between fetal and maternal tissue at mid-gestation, it undergoes fragmentation by the end of gestation. Thus, uterine and chorionic epithelial are directly apposed in some regions of the allantoplacenta, forming continuous cellular boundaries at the placental interface. During development, capillaries proliferate in both the uterine and chorioallantoic tissues. By late gestation, the interhemal diffusion distance has thinned in some areas to less than 2 microm through attenuation of the uterine and chorionic epithelia. Morphologically, the allantoplacenta is well adapted for its function in gas exchange. However, the presence of cytoplasmic vesicles, ribosomal ER, and mitochondria in the chorionic and uterine epithelial cells are consistent with the possibility of additional forms of placental exchange.     

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.     

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.