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Guppies in Trinidad range across aquatic environments with fish communities that vary in risk of predation. These communities are often discrete, separated by waterfalls, with high-predation communities downstream and low-predation communities upstream. This gradient is repeated in many rivers; in each one, we see the same divergence between guppy populations in life history, behavior, morphology, and physiology. We have shown that the agent of selection on the life history, behavior, and physiology in low-predation communities is high population density and the cascade of ecological effects that stems from it. In effect, guppy populations modify their ecosystem and, in so doing, impose selection on themselves and shape their own evolution, which further changes the ecosystem. Evolution unfolds rapidly in this system, which has enabled us to study the dynamics of the process, not just its end points. Those studies enable us to answer some very general questions in ecology and evolutionary biology.

Experimentally transplanting guppies to evolve in a novel, predator-free environment reveals that the direction of plasticity in gene expression is usually opposite to the direction of adaptive evolution; that is, those genes whose expression changes are disadvantageous are more strongly selected upon than those whose changes are advantageous. Effect of phenotypic plasticity on selection Phenotypic plasticity may have a role in the evolutionary adaptation of populations to changed environmental conditions, but it has not been clear whether it facilitates or hinders adaptation. These authors allow guppies to evolve in a novel predator-free environment and look at the resulting changes in gene expression. They see that the genes that evolve expression differences are not those that were adaptively phenotypically plastic, but those whose plasticity of gene expression was non-adaptive in the ancestral population. In other words, genes whose expression reacts to the environment in an advantageous way tend not to evolve in response to selection, whereas those whose expression changes are disadvantageous are strongly selected on. Phenotypic plasticity is the capacity for an individual genotype to produce different phenotypes in response to environmental variation 1 . Most traits are plastic, but the degree to which plasticity is adaptive or non-adaptive depends on whether environmentally induced phenotypes are closer or further away from the local optimum 2 , 3 , 4 . Existing theories make conflicting predictions about whether plasticity constrains or facilitates adaptive evolution 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 . Debate persists because few empirical studies have tested the relationship between initial plasticity and subsequent adaptive evolution in natural populations. Here we show that the direction of plasticity in gene expression is generally opposite to the direction of adaptive evolution. We experimentally transplanted Trinidadian guppies ( Poecilia reticulata ) adapted to living with cichlid predators to cichlid-free streams, and tested for evolutionary divergence in brain gene expression patterns after three to four generations. We find 135 transcripts that evolved parallel changes in expression within the replicated introduction populations. These changes are in the same direction exhibited in a native cichlid-free population, suggesting rapid adaptive evolution. We find 89% of these transcripts exhibited non-adaptive plastic changes in expression when the source population was reared in the absence of predators, as they are in the opposite direction to the evolved changes. By contrast, the remaining transcripts exhibiting adaptive plasticity show reduced population divergence. Furthermore, the most plastic transcripts in the source population evolved reduced plasticity in the introduction populations, suggesting strong selection against non-adaptive plasticity. These results support models predicting that adaptive plasticity constrains evolution 6 , 7 , 8 , whereas non-adaptive plasticity potentiates evolution by increasing the strength of directional selection 11 , 12 . The role of non-adaptive plasticity in evolution has received relatively little attention; however, our results suggest that it may be an important mechanism that predicts evolutionary responses to new environments.

Metabolic rates and life history strategies are both thought to set the “pace of life”, but whether they evolve in tandem is not well understood. Here, using a common garden experiment that compares replicate paired populations, we show that Trinidadian guppy ( Poecilia reticulata ) populations that evolved a fast-paced life history in high-predation environments have consistently higher metabolic rates than guppies that evolved a slow-paced life history in low-predation environments. Furthermore, by transplanting guppies from high- to low-predation environments, we show that metabolic rate evolves in parallel with the pace of life history, at a rapid rate, and in the same direction as found for naturally occurring populations. Together, these multiple lines of inference provide evidence for a tight evolutionary coupling between metabolism and the pace of life history. The ‘pace of life’ depends on both metabolic rate and life history traits; however, whether these evolve similarly in response to the environment is not clear. Here, Auer et al. show parallel evolution of metabolic rate and a suite of life history traits in response to predator environment in Trinidadian guppies.

The fish subfamily Poeciliinae (sensu Parenti, 1981) is widely distributed across the Western Hemisphere and a dominant component of the fish communities of Central America. Poeciliids have figured prominently in previous studies on the roles of dispersal and vicariance in shaping current geographic distributions. Most recently, Hrbek et al. combined a DNA-based phylogeny of the family with geological models to provide a biogeographic perspective that emphasized the role of both vicariance and dispersal. Here we expand on that effort with a database enlarged in the quantity of sequence represented per species, in the number of species included, and in an enlarged and more balanced representation of the order Cyprinodontiformes. We combine a robust timetree based upon multiple fossil calibrations with enhanced biogeographic analyses that include ancestral area reconstructions to provide a detailed biogeographic history of this clade. Key features of our results are that the family originated in South America, but its major diversification dates to a later colonization of Central America. We also resolve additional colonizations among South, Central and North America and the Caribbean and consider how this reconstruction contributes to our understanding of the mechanisms of dispersal.

Phenotypic plasticity is advantageous for organisms that live in variable environments. The digestive system is particularly plastic, responding to changes in diet. Gut length is the result of a trade-off between maximum nutrient absorption and minimum cost for its maintenance and it can be influenced by diet and by evolutionary history. We assessed variation in gut length of Trinidadian guppies (Poecilia reticulata) as a function of diet, season, ontogeny, and local adaptation. Populations of guppies adapted to different predation levels have evolved different life history traits and have different diets. We sampled guppies from sites with low (LP) and high predation (HP) pressure in the Aripo and Guanapo Rivers in Trinidad. We collected fish during both the dry and wet season and assessed their diet and gut length. During the dry season, guppies from HP sites fed mostly on invertebrates, while guppies in the LP sites fed mainly on detritus. During the wet season, the diet of LP and HP populations became very similar. We did not find strong evidence of an ontogenetic diet shift. Gut length was negatively correlated with the proportion of invertebrates in diet across fish from all sites, supporting the hypothesis that guppy digestive systems adapt in length to changes in diet. Population of origin also had an effect on gut length, as HP and LP fish maintained different gut lengths even in the wet season, when their diets were very similar and individuals in both types of populations fed mostly on detritus. Thus, both environment and population of origin influenced guppies gut length, but population of origin seemed to have a stronger effect. Our study also showed that, even in omnivorous fish, gut length adapted to different diets, being more evident when the magnitude of difference between animal and plant material in the diet was very large.

In live-bearing animal lineages, the evolution of the placenta is predicted to create an arena for genomic conflict during pregnancy, drive patterns of male sexual selection, and increase the rate of speciation. Here we test these predictions of the viviparity driven conflict hypothesis (VDCH) in live-bearing poecilid fishes, a group showing multiple independent origins of placentation and extreme variation in male sexually selected traits. As predicted, male sexually selected traits are only gained in lineages that lack placentas; while there is little or no influence of male traits on the evolution of placentas. Both results are consistent with the mode of female provisioning governing the evolution of male attributes. Moreover, it is the presence of male sexually selected traits (pre-copulatory), rather than placentation (post-copulatory), that are associated with higher rates of speciation. These results highlight a causal interaction between female reproductive mode, male sexual selection and the rate of speciation, suggesting a role for conflict in shaping diverse aspects of organismal biology. The viviparity driven conflict hypothesis predicts the evolution of the placenta will suppress the evolution of traits associated with pre-copulatory mate choice and accelerate speciation rate. Furness et al. support the former and disprove the latter predictions with comparative analyses of the poecilid fishes.

Theory suggests evolutionary change can significantly influence and act in tandem with ecological forces via ecological-evolutionary feedbacks. This theory assumes that significant evolutionary change occurs over ecologically relevant timescales and that phenotypes have differential effects on the environment. Here we test the hypothesis that local adaptation causes ecosystem structure and function to diverge. We demonstrate that populations of Trinidadian guppies (Poecilia reticulata), characterized by differences in phenotypic and population-level traits, differ in their impact on ecosystem properties. We report results from a replicated, common garden mesocosm experiment and show that differences between guppy phenotypes result in the divergence of ecosystem structure (algal, invertebrate, and detrital standing stocks) and function (gross primary productivity, leaf decomposition rates, and nutrient flux). These phenotypic effects are further modified by effects of guppy density. We evaluated the generality of these effects by replicating the experiment using guppies derived from two independent origins of the phenotype. Finally, we tested the ability of multiple guppy traits to explain observed differences in the mesocosms. Our findings demonstrate that evolution can significantly affect both ecosystem structure and function. The ecosystem differences reported here are consistent with patterns observed across natural streams and argue that guppies play a significant role in shaping these ecosystems.

The empirical study of natural selection reveals that adaptations often involve trade‐offs between competing functions. Because natural selection acts on whole organisms rather than isolated traits, adaptive evolution may be constrained by the interaction between traits that are functionally integrated. Yet, few attempts have been made to characterize how and when such constraints are manifested or whether they limit the adaptive divergence of populations. Here we examine the consequences of adaptive life‐history evolution on locomotor performance in the live‐bearing guppy. In response to increased predation from piscivorous fish, Trinidadian guppies evolve an increased allocation of resources toward reproduction. These populations are also under strong selection for rapid fast‐start swimming performance to evade predators. Because embryo development increases a female’s wet mass as she approaches parturition, an increased investment in reproductive allocation should impede fast‐start performance. We find evidence for adaptive but constrained evolution of fast‐start swimming performance in laboratory trials conducted on second‐generation lab‐reared fish. Female guppies from high‐predation localities attain a faster acceleration and velocity and travel a greater distance during fast‐start swimming trials. However, velocity and distance traveled decline more rapidly over the course of pregnancy in these same females, thus reducing the magnitude of divergence in swimming performance between high‐ and low‐predation populations. This functional trade‐off between reproduction and swimming performance reveals how different aspects of the phenotype are integrated and highlights the complexity of adaptation at the whole‐organism level.