Post-fertilization Maternal Provisioning Research Articles

Can females differentially allocate resources to offspring sired by different males?

Abstract The viviparity-driven conflict hypothesis postulates that the evolution of matrotrophy (postfertilization maternal provisioning) will result in a shift from a pre- to postcopulatory mate choice and thus accelerate the evolution of postcopulatory reproductive isolation. Here, we perform artificial insemination experiments on Heterandria formosa, a matrotrophic poeciliid fish, to probe for evidence of postcopulatory female choice. We established laboratory populations from Wacissa River (WR) and Lake Jackson (LJ). The WR females normally produce larger offspring than the LJ females. We artificially inseminated females with sperm from each population or from both populations simultaneously. When LJ females were inseminated with sperm from WR and LJ males, they allocated fewer resources to WR-sired offspring than when they were inseminated with WR sperm alone. The LJ females carrying developing offspring sired by males from different populations were thus able to discriminate against non-resident males when allocating resources to developing young. The WR females, which normally produce larger offspring than LJ females, did not discriminate among males from different localities. These findings provide insights into the ability of females from one population to exercise a form of postcopulatory mate selection.

Examination of the Trexler-DeAngelis Model of Maternal Provisioning Reveals That Matrotrophy Is Costly

The evolution of matrotrophy (post-fertilization maternal provisioning to developing embryos) has been explained through several hypotheses. Trexler and DeAngelis proposed in 2003 a theoretical model that defines the ecological conditions under which matrotrophy would be favored over lecithotrophy (pre-fertilization maternal provisioning). According to this model, matrotrophy offers a selective advantage in environments with abundant and constantly available food, whereas environments with limited and fluctuating food resources should instead promote a lecithotrophic mode of maternal provisioning. This model also proposes that matrotrophy entails the consequence of leaner reproductive females and in turn shorter lifespans. In this study, we examined the Trexler-DeAngelis model using data from 45 populations of five viviparous species from the fish genus Poeciliopsis (family Poeciliidae). We used the matrotrophy index (MI) as a measure of post-fertilization maternal provisioning, and the index of stomach fullness and individual body condition (BC) as proxies for food availability. We also estimated the magnitude of fluctuations in food availability by calculating the temporal variances of these two proxies. Neither abundant nor constantly available food were associated with greater degrees of matrotrophy, which fails to support the predictions of the Trexler-DeAngelis model with respect to the ecological drivers of increased post-fertilization provisioning to embryos. Nonetheless, in all five species we observed that females with greater degrees of matrotrophy had poorer BC compared to females that provided less nutrients to embryos after fertilization. This finding is consistent with one of the expected consequences of advanced matrotrophy according to the Trexler-DeAngelis model, namely, a detriment to the nutritional status of females. Our study provides compelling evidence that gestating females experience a trade-off between post-fertilization provisioning to embryos and self-maintenance, revealing in turn that matrotrophy is a costly reproductive strategy.

Maternal size and body condition predict the amount of post-fertilization maternal provisioning in matrotrophic fish.

Maternal effects often provide a mechanism for adaptive transgenerational phenotypic plasticity. The maternal phenotype can profoundly influence the potential for such environmentally induced adjustments of the offspring phenotype, causing correlations between offspring and maternal traits. Here, we study potential effects of the maternal phenotype on offspring provisioning prior to and during gestation in the matrotrophic live‐bearing fish species Poeciliopsis retropinna. Specifically, we examine how maternal traits such as body fat, lean mass, and length relate to pre‐ (i.e., allocation to the egg prior to fertilization) and post‐fertilization (i.e., allocation to the embryo during pregnancy) maternal provisioning and how this ultimately affects offspring size and body composition at birth. We show that pre‐ and post‐fertilization maternal provisioning is associated with maternal length and body fat, but not with maternal lean mass. Maternal length is proportionally associated with egg mass at fertilization and offspring mass at birth, notably without changing the ratio of pre‐ to post‐fertilization maternal provisioning. This ratio, referred to as the matrotrophy index (MI), is often used to quantify the level of matrotrophy. By contrast, the proportion of maternal body fat is positively associated with post‐fertilization, but not pre‐fertilization, maternal provisioning and consequently is strongly positively correlated with the MI. We furthermore found that the composition of embryos changes throughout pregnancy. Females invest first in embryo lean mass, and then allocate fat reserves to embryos very late in pregnancy. We argue that this delay in fat allocation may be adaptive, because it delays an unnecessary high reproductive burden to the mother during earlier stages of pregnancy, potentially leading to a more slender body shape and improved locomotor performance. In conclusion, our study suggests that (a) offspring size at birth is a plastic trait that is predicted by both maternal length and body fat, and (b) the MI is a plastic trait that is predicted solely by the proportion of maternal body fat. It herewith provides new insights into the potential maternal causes and consequences of embryo provisioning during pregnancy in matrotrophic live‐bearing species.

Tissue-Specific Transcriptome for Poeciliopsis prolifica Reveals Evidence for Genetic Adaptation Related to the Evolution of a Placental Fish.

The evolution of the placenta is an excellent model to examine the evolutionary processes underlying adaptive complexity due to the recent, independent derivation of placentation in divergent animal lineages. In fishes, the family Poeciliidae offers the opportunity to study placental evolution with respect to variation in degree of post-fertilization maternal provisioning among closely related sister species. In this study, we present a detailed examination of a new reference transcriptome sequence for the live-bearing, matrotrophic fish, Poeciliopsis prolifica, from multiple-tissue RNA-seq data. We describe the genetic components active in liver, brain, late-stage embryo, and the maternal placental/ovarian complex, as well as associated patterns of positive selection in a suite of orthologous genes found in fishes. Results indicate the expression of many signaling transcripts, “non-coding” sequences and repetitive elements in the maternal placental/ovarian complex. Moreover, patterns of positive selection in protein sequence evolution were found associated with live-bearing fishes, generally, and the placental P. prolifica, specifically, that appear independent of the general live-bearer lifestyle. Much of the observed patterns of gene expression and positive selection are congruent with the evolution of placentation in fish functionally converging with mammalian placental evolution and with the patterns of rapid evolution facilitated by the teleost-specific whole genome duplication event.

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 to 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 to 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 likely resulted from selective responses to the local conditions.

Predation’s Role in Life-History Evolution of a Livebearing Fish and a Test of the Trexler-DeAngelis Model of Maternal Provisioning

Populations experiencing consistent differences in predation risk and resource availability are expected to follow divergent evolutionary trajectories. For example, live-history theory makes specific predictions for how predation should drive life-history evolution, and according to the Trexler-DeAngelis model for the evolution of matrotrophy, postfertilization maternal provisioning is most likely to evolve in environments with consistent, high levels of resource availability. Using the model system of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes with and without the piscivorous bigmouth sleeper (Gobiomorus dormitor), we provide some of the strongest tests of these predictions to date, as resource availability does not covary with predation regime in this system, and we examine numerous (14) isolated natural populations. We found clear evidence for the expected life-history divergence between predation regimes and empirical support of the Trexler-DeAngelis model. Moreover, based on molecular and lab-rearing data, our study offers strong evidence for convergent evolution of similar life histories in similar predation regimes, largely matching previous phenotypic patterns observed in other poeciliid lineages (Brachyrhaphis spp., Poecilia reticulata), and further supports the notion that matrotrophy is most likely to evolve in stable high-resource environments.

Analysis of Expressed Sequence Tags from the Placenta of the Live-Bearing Fish Poeciliopsis (Poeciliidae)

Matrotrophic fish in the genus Poeciliopsis (Poeciliidae) have a placenta-like structure used in postfertilization maternal provisioning of the developing embryo. To understand better the structure and function of the Poeciliopsis placenta, we derived cDNA libraries from the maternal follicular placenta of 2 matrotrophic Poeciliopsis sister species, P. turneri and P. presidionis. These species inherited their placenta from a common ancestor and represent one of 3 independent origins of placentas in Poeciliopsis. Expressed sequence tags (ESTs) were generated and putative function was determined using BLASTX homology searches and Gene Ontology (GO) annotation. Reverse transcription-polymerase chain reaction was used to verify placenta tissue expression of a putative candidate gene, alpha-2 macroglobulin. In total, 1956 (71.5% of the total submitted ESTs) and 924 (71.0% of the total submitted ESTs) unique transcripts were identified for the P. turneri and P. presidionis placenta, respectively. Homology search and GO annotation revealed putative genes whose products may be involved in specific transport functions of the maternal follicle. These putative genes are excellent candidates for future research on the evolution of the placenta. We discuss our results in light of the parent-offspring conflict theory of placental evolution and in terms of the Poeciliid placenta structure and function.

Pre‐ and post‐fertilization maternal provisioning in livebearing fish species and their hybrids (Poeciliidae: Poeciliopsis)

Summary 1. Viviparous organisms vary greatly in their level of post-fertilization maternal provisioning and extensive provisioning (including very complex placentas) has evolved dozens of times in vertebrates. Through the use of species representing transitional states we aim to explore and develop empirically supported hypotheses that explain how such a complex trait has evolved. 2. In this study, we investigated the life histories and patterns of post-fertilization maternal provisioning in naturally occurring, all-female, hybrids between Poeciliopsis monacha , a viviparous species that produces large eggs and nourishes its embryos via stored yolk (lecithotrophy) and P. lucida , which produces small eggs and nourishes its embryos after fertilization via a follicular placenta (matrotrophy). Hybrids can be diploid or triploid, leading to different levels of gene dosage from the parental species. 3. We found that the extent of superfetation and average brood size of the hybrids did not differ significantly from their sexual parental species even though the latter was much lower in the hybrids. Moreover, the allodiploid, P. monacha-lucida , has intermediate sized eggs, whereas the allotriploid, P. monacha-monacha-lucida , produces eggs of similar size to those of P. monacha . The degree of post-fertilization maternal provisioning was unrelated to genomic dosages, with wild-caught hybrids being lecithotrophic, as seen in the maternal species ( P. monacha ). 4. Our results with naturally occurring P. monacha-lucida hybrids differed from those obtained with laboratory-synthesized hybrid clones, which were either lecithotrophic or weakly matrotrophic. Consequently, we propose two non-mutually exclusive hypotheses to explain why lecithotrophic clones might be favoured in the wild. One hypothesis suggests that lecithotrophic hybrids minimize competition with the matrotrophic paternal sexual species from which they require sperm to reproduce. Alternatively, we propose that natural selection has eliminated matrotrophic hybrids that suffer from intergenomic conflict in the degree of post-fertilization maternal provisioning. 5. We have thus identified an empirical system and developed testable hypotheses that will help elucidate the selective pressures that caused the evolution of post-fertilization maternal provisioning and potentially provide an opportunity to explore how epigenetic factors (e.g., intergenomic conflict) might influence this complex trait.

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.