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In poeciliid fish, the evolution of the placenta is associated with polyandry in females and correlates with a suite of phenotypic and behavioural traits in males. Consequences of placenta evolution Females laying eggs for external fertilization have no control over the quality of the offspring, and must rely on proxies of male quality such as courtship and display traits. Evolutionary theory holds that all this changed with the advent of the placenta: with low-cost eggs incubated internally, a mother can hedge her bets, inspecting the genetic quality of her mates directly and provisioning her embryos accordingly. The resulting mother–offspring conflict is expected to lead to polyandry (females mating with multiple males) and to males that are smaller, less showy and more prone to opportunistic or 'sneaky' mating. Here Bart Pollux et al . test these ideas by looking at the Poecilidae — guppies and their relatives — a family of fish in which the various species show all varieties of internal and external fertilization, and in which the placenta has evolved at least eight times independently. This approach allows the authors to confirm that the evolution of the placenta is associated with polyandry in females, and smaller, less showy males that have longer penises to facilitate more opportunities for opportunistic mating. 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 1 , 2 , 3 , 4 . 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 2 . 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 5 , 6 . 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.

Two ways in which organisms adapt to variable environments are phenotypic plasticity and bet-hedging. Theory suggests that bet-hedging is expected to evolve in unpredictable environments for which reliable cues indicative of future conditions (or season length) are lacking. Alternatively, if reliable cues exist indicating future conditions, organisms will be under selection to produce the most appropriate phenotype—that is, adaptive phenotypic plasticity. Here, we experimentally test which of these modes of adaptation are at play in killifish that have evolved an annual life cycle. These fish persist in ephemeral pools that completely dry each season through the production of eggs that can remain in developmental arrest, or diapause, buried in the soil, until the following rainy season. Consistent with diversified bet-hedging (a risk spreading strategy), we demonstrate that the eggs of the annual killifish Nothobranchius furzeri exhibit variation at multiple levels—whether or not different stages of diapause are entered, for how long diapause is entered, and the timing of hatching—and this variation persists after controlling for both genetic and environmental sources of variation. However, we show that phenotypic plasticity is also present in that the proportion of eggs that enter diapause is influenced by environmental factors (temperature and light level) that vary seasonally. In nature there is typically a large parameter zone where environmental cues are somewhat correlated with seasonality, but not perfectly so, such that it may be advantageous to have a combination of both bet-hedging and plasticity.

Annual killifish adapted to life in seasonally ephemeral water-bodies exhibit desiccation resistant eggs that can undergo diapause, a period of developmental arrest, enabling them to traverse the otherwise inhospitable dry season. Environmental cues that potentially indicate the season can govern whether eggs enter a stage of diapause mid-way through development or skip this diapause and instead undergo direct development. We report, based on construction of a supermatrix phylogenetic tree of the order Cyprinodontiformes and a battery of comparative analyses, that the ability to produce diapause eggs evolved independently at least six times within African and South American killifish. We then show in species representative of these lineages that embryos entering diapause display significant reduction in development of the cranial region and circulatory system relative to direct-developing embryos. This divergence along alternative developmental pathways begins mid-way through development, well before diapause is entered, during a period of purported maximum developmental constraint (the phylotypic period). Finally, we show that entering diapause is accompanied by a dramatic reduction in metabolic rate and concomitant increase in long-term embryo survival. Morphological divergence during the phylotypic period thus allows embryos undergoing diapause to conserve energy by shunting resources away from energetically costly organs thereby increasing survival chances in an environment that necessitates remaining dormant, buried in the soil and surrounded by an eggshell for much of the year. Our results indicate that adaptation to seasonal aquatic environments in annual killifish imposes strong selection during the embryo stage leading to marked diversification during this otherwise conserved period of vertebrate development.

Nothobranchius furzeri is an important new model organism. This Protocol aims to help laboratories establish healthy breeding colonies of this species and to standardize husbandry methods, which differ from those for other model fish because of dry incubation of the eggs. Turquoise killifish, Nothobranchius furzeri , have an intrinsically short life span, with a median life span of <6 months and a maximum (90%) life span of 9 months. This short life span, which is unique among vertebrates, evolved naturally and has resulted in N. furzeri becoming a widely used laboratory model species in aging research and other disciplines. Here, we describe a protocol for the maintenance and breeding of the species under laboratory conditions. We provide details for egg incubation, hatching, everyday care of juvenile and adult fish, breeding and treatment of most common diseases. Emphasis is given to the fact that the requirements of N. furzeri substantially differ from those of other fish model taxa; N. furzeri live brief lives and in nature undergo nonaquatic embryo development, with consequences for their laboratory culture.

The turquoise killifish, Nothobranchius furzeri, is a promising vertebrate model in ageing research and an emerging model organism in genomics, regenerative medicine, developmental biology and ecotoxicology. Its lifestyle is adapted to the ephemeral nature of shallow pools on the African savannah. Its rapid and short active life commences when rains fill the pool: fish hatch, grow rapidly and mature in as few as two weeks, and then reproduce daily until the pool dries out. Its embryos then become inactive, encased in the dry sediment and protected from the harsh environment until the rains return. This invertebrate-like life cycle (short active phase and long developmental arrest) combined with a vertebrate body plan provide the ideal attributes for a laboratory animal.

Although first described in 1880, Kryptolebias marmoratus avoided scientific scrutiny until 1961, when it was identified as the only known selfing hermaphroditic vertebrate. The subsequent intense interest in this fish as a laboratory animal, continuing to this day, might explain the paucity of wild collections, but our collective knowledge now suggests that the inherent difficulty of wild collection is more a matter of “looking in all the wrong places.” Long thought to be rare in the mangroves, and it is rare in certain human-impacted habitats, K. marmoratus can be quite abundant, but in microhabitats not typically targeted by ichthyologists: ephemeral pools at higher elevations in the swamp, crab burrows, and other fossorial or even terrestrial haunts. Field studies of this enigmatic fish have revealed almost amphibious behaviors. During emersion these fish tolerate extended dry periods. In water, they are exposed to temperature extremes, high levels of hydrogen sulfide, and depleted dissolved oxygen. Finally, their catholic diet and a geographically variable sex life completes a portrait of an unusual animal. A clearer picture is emerging of adult life, with initial population density estimates now known and some indication of high population turnover in burrows, but juvenile habitat and adult oviposition sites remain unknown.

Life span and aging are substantially modified by natural selection. Across species, higher extrinsic (environmentally related) mortality (and hence shorter life expectancy) selects for the evolution of more rapid aging. However, among populations within species, high extrinsic mortality can lead to extended life span and slower aging as a consequence of condition-dependent survival. Using within-species contrasts of eight natural populations of Nothobranchius fishes in common garden experiments, we demonstrate that populations originating from dry regions (with short life expectancy) had shorter intrinsic life spans and a greater increase in mortality with age, more pronounced cellular and physiological deterioration (oxidative damage, tumor load), and a faster decline in fertility than populations from wetter regions. This parallel intraspecific divergence in life span and aging was not associated with divergence in early life history (rapid growth, maturation) or pace-of-life syndrome (high metabolic rates, active behavior). Variability across four study species suggests that a combination of different aging and life-history traits conformed with or contradicted the predictions for each species. These findings demonstrate that variation in life span and functional decline among natural populations are linked, genetically underpinned, and can evolve relatively rapidly.

Species richness is distributed unevenly across the tree of life and this may be influenced by the evolution of novel phenotypes that promote diversification. Viviparity has originated B150 times in vertebrates and is considered to be an adaptation to highly variable environments. Likewise, possessing an annual life cycle is common in plants and insects, where it enables the colonization of seasonal environments, but rare in vertebrates. The extent to which these reproductive life-history traits have enhanced diversification and their relative importance in the process remains unknown. We show that convergent evolution of viviparity causes bursts of diversification in fish. We built a phylogenetic tree for Cyprino-dontiformes, an order in which both annualism and viviparity have arisen, and reveal that while both traits have evolved multiple times, only viviparity played a major role in shaping the patterns of diversity. These results demonstrate that changes in reproductive life-history strategy can stimulate diversification.

Ecological invasions, where non-native species spread to new areas, grow to high densities and have large, negative impacts on ecological communities, are a major worldwide problem. Recent studies suggest that one of the key mechanisms influencing invasion dynamics is personality-dependent dispersal: the tendency for dispersers to have a different personality type than the average from a source population. We examined this possibility in the invasive mosquitofish (Gambusia affinis). We measured individual tendencies to disperse in experimental streams and several personality traits: sociability, boldness, activity and exploration tendency before and three weeks after dispersal. We found that mosquitofish display consistent behavioural tendencies over time, and significant positive correlations between all personality traits. Most notably, sociability was an important indicator of dispersal distance, with more asocial individuals dispersing further, suggesting personality-biased dispersal on an invasion front. These results could have important ecological implications, as invasion by a biased subset of individuals is likely to have different ecological impacts than invasion by a random group of colonists.

Sex ratio and sexual dimorphism have long been of interest in population and evolutionary ecology, but consequences for communities and ecosystems remain untested. Sex ratio could influence ecological conditions whenever sexual dimorphism is associated with ecological dimorphism in species with strong ecological interactions. We tested for ecological implications of sex ratio variation in the sexually dimorphic western mosquitofish, Gambusia affinis. This species causes strong pelagic trophic cascades and exhibits substantial variation in adult sex ratios. We found that female-biased populations induced stronger pelagic trophic cascades compared with male-biased populations, causing larger changes to key community and ecosystem responses, including zooplankton abundance, phytoplankton abundance, productivity, pH and temperature. The magnitude of such effects indicates that sex ratio is important for mediating the ecological role of mosquitofish. Because both sex ratio variation and sexual dimorphism are common features of natural populations, our findings should encourage broader consideration of the ecological significance of sex ratio variation in nature, including the relative contributions of various sexually dimorphic traits to these effects.