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.
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.
1. The ability to adjust the allocation of energy to maintenance, growth and reproduction in response to fluctuations in resource availability, in a way that enhances fitness, is thought to depend on the mode of maternal provisioning. 2. We manipulated food availability in the matrotrophic, livebearing fish Phalloptychus januarius (Poeciliidae) to examine patterns of allocation under fluctuating resource conditions. 3. We observed an asynchrony in the adjustment of offspring traits in response to changes in food availability. A reduction in food availability caused an immediate reduction in allocation of energy to offspring size and lipid content at birth, but a delayed reduction in offspring number (fecundity). Similarly, an increase in food availability caused an immediate increase in offspring size and lipid content and a delayed increase in fecundity. This asynchrony is thought to be inherent to matrotrophy, limiting a female's ability to attain an optimal fitness in fluctuating resource environments, regardless of whether food availability changes from high to low, or low to high. 4. We found no evidence for embryo abortion under low food conditions. All developing offspring were retained, yet were smaller at birth. Furthermore, although females carried large fat reserves, these were rapidly depleted during low food conditions and were not sufficient to fully buffer gestating females or their developing offspring against the detrimental effects of reduced food availability. 5. Our study shows that matrotrophy is likely to be a maladaptive strategy in environments that are characterized by fluctuations in resource availability. It further suggests that matrotrophy is most likely to evolve in high and stable resource environments.
Many aquatic and riparian plant species are characterized by the ability to reproduce both sexually and asexually. Yet, little is known about how spatial variation in sexual and asexual reproduction affects the genotypic diversity within populations of aquatic and riparian plants. We used six polymorphic microsatellites to examine the genetic diversity within and differentiation among 17 populations (606 individuals) of Sparganium emersum, in two Dutch-German rivers. Our study revealed a striking difference between rivers in the mode of reproduction (sexual vs. asexual) within S. emersum populations. The mode of reproduction was strongly related to locally reigning hydrodynamic conditions. Sexually reproducing populations exhibited a greater number of multilocus genotypes compared to asexual populations. The regional population structure suggested higher levels of gene flow among sexually reproducing populations compared to clonal populations. Gene flow was mainly mediated via hydrochoric dispersal of generative propagules (seeds), impeding genetic differentiation among populations even over river distances up to 50 km. Although evidence for hydrochoric dispersal of vegetative propagules (clonal plant fragments) was found, this mechanism appeared to be relatively less important. Bayesian-based assignment procedures revealed a number of immigrants, originating from outside our study area, suggesting intercatchment plant dispersal, possibly the result of waterfowl-mediated seed dispersal. This study demonstrates how variation in local environmental conditions in river systems, resulting in shifting balances of sexual vs. asexual reproduction within populations, will affect the genotypic diversity within populations. This study furthermore cautions against generalizations about dispersal of riparian plant species in river systems.
1. In river ecosystems, populations are continuously subjected to unidirectional downstream currents resulting in a downstream movement of populations. To ensure long-term population persistence in rivers, organisms must have a mechanism for upstream dispersal, which allows them to re-colonise upstream areas. 2. In this study we assessed differences in the potential for endozoochorous seed dispersal of Sparganium emersum and Sagittaria sagittifolia, two aquatic plant species with different seed morphologies, by mallard (Anas platyrhynchos) and teal (Anas crecca), two duck species with different body weights. 3. We found no significant differences in seed retrieval (the proportion of ingested seeds retrieved after gut passage) and seed retention time (time between seed ingestion and retrieval), between mallard and teal, despite the difference in body weights. We did find a significantly higher germination (%) over retention time of S. emersum seeds retrieved from teal compared with mallard, most likely related to a more efficient removal of the seed coat during passage through the gut of teal. 4. There were large differences between S. emersum versus S. sagittifolia in: (i) seed retrieval (22.65 ± 20.8% versus 1.60 ± 2.4%, respectively); (ii) seed retention time in duck gut, with a maximum of 60 h versus 12 h; (iii) the effect of gut passage on seed germination, with an increase of approximately 35% versus a decrease of 25%; and (iv) the effect of gut passage on seed germination rate, with an acceleration of 10 days versus a delay of 3 days on average. The results show that S. emersum has a higher potential for endozoochorous dispersal by ducks and postdispersal establishment than S. sagittifolia. 5. We propose that, in rivers, bird-mediated seed dispersal may promote re-colonisation of upstream areas, enabling long-term plant population persistence.
1. River systems offer special environments for the dispersal of aquatic plants because of the unidirectional (downstream) flow and linear arrangement of suitable habitats. 2. To examine the effect of this flow on microevolutionary processes in the unbranched bur-reed (Sparganium emersum) we studied the genetic variation within and among nine (sub)populations along a 103 km stretch of the Niers River (Germany-The Netherlands), using amplified fragment length polymorphisms. 3. Genetic diversity in S. emersum populations increased significantly downstream, suggesting an effect of flow on the pattern of intrapopulation genetic diversity. 4. Gene flow in the Niers River is asymmetrically bidirectional, with gene flow being approximately 3.5 times higher in a downstream direction. The observed asymmetry is probably caused by frequent hydrochoric dispersal towards downstream locations on the one hand, and sporadic zoochoric dispersal in an upstream direction on the other. The spread of vegetative propagules (leaf and stem fragments) is probably not an important mode of dispersal for S. emersum, suggesting that gene flow is mainly via seed dispersal. Realized dispersal distances exceeded 60 km, revealing a potential for long-distance dispersal in S. emersum. 5. There was no correlation between geographical and genetic distances among the nine S. emersum populations (i.e. no isolation by distance), which may be due to the occurrence of long-distance dispersal and ⁄ or colonization and extinction dynamics in the Niers River. 6. Overall, the genetic population structure and regional dispersal patterns of S. emersum in the Niers River are best explained by a linear metapopulation model. Our study shows that flow can exert a strong influence on population genetic processes of plants inhabiting stream systems.
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