Genomic approaches with natural fish populations

Natural populations v. inbred stocks provide a much richer resource for identifying the effects of nucleotide substitutions because natural populations have greater polymorphism. Additionally, natural populations offer an advantage over most common research organisms because they are subject to natural selection, and analyses of these adaptations can be used to identify biologically important changes. Among fishes, these analyses are enhanced by having a wide diversity of species (>28 000 species, more than any other group of vertebrates) living in a huge range of environments (from below freezing to > 46° C, in fresh water to salinities >40 ppt.). Moreover, fishes exhibit many different life‐history and reproductive strategies and have many different phenotypes and social structures. Although fishes provide numerous advantages over other vertebrate models, there is still a dearth of available genomic tools for fishes. Fishes make up approximately half of all known vertebrate species, yet <0·2% of fish species have significant genomic resources. Nonetheless, genomic approaches with fishes have provided some of the first measures of individual variation in gene expression and insights into environmental and ecological adaptations. Thus, genomic approaches with natural fish populations have the potential to revolutionize fundamental studies of diverse fish species that offer myriad ecological and evolutionary questions.     

Strong links between genomic and anatomical diversity in both mammalian olfactory chemosensory systems

Mammalian olfaction comprises two chemosensory systems: the odorant-detecting main olfactory system (MOS) and the pheromone-detecting vomeronasal system (VNS). Mammals are diverse in their anatomical and genomic emphases on olfactory chemosensation, including the loss or reduction of these systems in some orders. Despite qualitative evidence linking the genomic evolution of the olfactory systems to specific functions and phenotypes, little work has quantitatively tested whether the genomic aspects of the mammalian olfactory chemosensory systems are correlated to anatomical diversity. We show that the genomic and anatomical variation in these systems is tightly linked in both the VNS and the MOS, though the signature of selection is different in each system. Specifically, the MOS appears to vary based on absolute organ and gene family size while the VNS appears to vary according to the relative proportion of functional genes and relative anatomical size and complexity. Furthermore, there is little evidence that these two systems are evolving in a linked fashion. The relationships between genomic and anatomical diversity strongly support a role for natural selection in shaping both the anatomical and genomic evolution of the olfactory chemosensory systems in mammals.     

On the relevance of using laboratory selection to study the adaptive value of circadian clocks

The phrase ‘as sure as night comes after day’ highlights the most conspicuous phenomenon on earth (i.e. the daily cycling of geophysical factors). It is hypothesized that life‐forms on earth have evolved timekeeping mechanisms (circadian clocks) as adaptations to cope with such cyclic variations in their environment and, to test this hypothesis, diverse strategies have been employed. In this review, these different approaches, including comparative, clinal, ecology and/or trait manipulation and laboratory selection strategies are discussed, aiming to evaluate the adaptive value of circadian clocks. The limitations of each of these methods are assessed, and it is suggested that laboratory selection is an ideal, potent and suitable strategy for examining whether circadian clocks are indeed adaptations. In support of this, laboratory selection strategies are highlighted and critically reviewed in a discussion of studies that demonstrate the evolution of circadian clocks and life‐history traits in response to selection for the timing of rhythmic behaviours, as well as those studies that demonstrate the evolution of circadian clocks in response to selection for life‐history traits. Finally, newer approaches are proposed that involve the use of mutants, simultaneous manipulation of multiple environmental factors and genomic technologies in conjunction with laboratory selection to further explore the adaptive significance of circadian clocks.     

How genomic and developmental dynamics affect evolutionary processes

Evolutionary genetics is concerned with natural selection and neutral drift, to the virtual exclusion of almost everything else. In its current focus on DNA variation, it reduces phenotypes to symbols. Varying phenotypes, however, are the units of evolution, and, if we want a comprehensive theory of evolution, we need to consider both the internal and external evolutionary forces that shape the development of phenotypes. Genetic systems are redundant, modular and subject to a variety of genomic mechanisms of "turnover" (transposition, gene conversion, unequal crossingover, slippage and so on). As such the construction and spread of novel combinations of modules by turnover, in particular within gene promoters, contributes significantly to the evolution of phenotypes. Furthermore, redundancy, turnover and modularity lead to ever more complex networks of genetic interactions and ever more functions for a given module. The significant interaction between genomic turnover and natural selection leads to a molecular coevolution between interacting modules and hence facilitates the establishment of biological novelties.     

Opsin Evolution in Damselfish: Convergence, Reversal, and Parallel Evolution Across Tuning Sites

The visual system plays a role in nearly every aspect of an organism??s life history, and there is a direct link between visual pigment phenotypes and opsin genotypes. In previous studies of African cichlid fishes, we found evidence for positive selection among some opsins, with sequence variation greatest for opsins producing the shortest and longest wavelength visual pigments. In this study, we examined opsin evolution in the closely related damselfish family (Pomacentridae), a group of reef fishes that are distributed widely and have a documented fossil record of at least 50?million years (MY). We found increased functional variation in the protein sequences of opsins at the short- and long-wavelength ends of the visual spectrum, in agreement with the African cichlids, despite an order of magnitude difference in the ages of the two radiations. We also reconstructed amino acid substitutions across opsin tuning sites. These reconstructions indicated multiple instances of parallel evolution, at least one definitive case of convergent evolution, and one evolutionary reversal. Our findings show that the amino acids at spectral tuning sites are labile evolutionarily, and that the same codons evolve repeatedly. These findings emphasize that the aquatic light environment can shape opsin sequence evolution. They further show that phylogenetic approaches can provide important insights into the mechanisms by which natural selection ??tinkers?? with phenotypes.     

Functional genomics of life history variation in a butterfly metapopulation

In fragmented landscapes, small populations frequently go extinct and new ones are established with poorly understood consequences for genetic diversity and evolution of life history traits. Here, we apply functional genomic tools to an ecological model system, the well-studied metapopulation of the Glanville fritillary butterfly. We investigate how dispersal and colonization select upon existing genetic variation affecting life history traits by comparing common-garden reared 2-day adult females from new populations with those from established older populations. New-population females had higher expression of abdomen genes involved in egg provisioning and thorax genes involved in the maintenance of flight muscle proteins. Physiological studies confirmed that new-population butterflies have accelerated egg maturation, apparently regulated by higher juvenile hormone titer and angiotensin converting enzyme mRNA, as well as enhanced flight metabolism. Gene expression varied between allelic forms of two metabolic genes (Pgi and Sdhd), which themselves were associated with differences in flight metabolic rate, population age and population growth rate. These results identify likely molecular mechanisms underpinning life history variation that is maintained by extinction-colonization dynamics in metapopulations.     

Genome-wide variation in the human and fruitfly: a comparison

Average levels of nucleotide diversity are ten-fold lower in humans than in the fruitfly, Drosophila melanogaster. Despite this difference, apparently as a result of a lower population size, patterns of genomic diversity are strikingly similar in being correlated with local rates of recombination, and influenced by similar interactions between positive natural selection and recombination. Both species also show lower levels of variation on average in non-African compared to African populations, reflecting a similar evolutionary history and perhaps both natural selection and founder effects in new environments.     

Among‐year variation in selection during early life stages and the genetic basis of fitness in Arabidopsis thaliana

Incomplete information regarding both selection regimes and the genetic basis of fitness limits our understanding of adaptive evolution. Among‐year variation in the genetic basis of fitness is rarely quantified, and estimates of selection are typically based on single components of fitness, thus potentially missing conflicting selection acting during other life‐history stages. Here, we examined among‐year variation in selection on a key life‐history trait and the genetic basis of fitness covering the whole life cycle in the annual plant Arabidopsis thaliana. We planted freshly matured seeds of >200 recombinant inbred lines (RILs) derived from a cross between two locally adapted populations (Italy and Sweden), and both parental genotypes at the native site of the Swedish population in three consecutive years. We quantified selection against the nonlocal Italian genotype, mapped quantitative trait loci (QTL) for fitness and its components, and quantified selection on timing of germination during different life stages. In all 3 years, the local Swedish genotype outperformed the nonlocal Italian genotype. However, both the contribution of early life stages to relative fitness, and the effects of fitness QTL varied among years. Timing of germination was under conflicting selection through seedling establishment vs. adult survival and fecundity, and both the direction and magnitude of net selection varied among years. Our results demonstrate that selection during early life stages and the genetic basis of fitness can vary markedly among years, emphasizing the need for multiyear studies considering the whole life cycle for a full understanding of natural selection and mechanisms maintaining local adaptation.     

Optimal age of maturity in fluctuating environments under r‐ and K‐selection

Optimality models for evolution of life histories have shown that increased environmental stochasticity promotes early age of maturity. Here we argue that if r‐selection for early maturation implies a tradeoff making those phenotypes more sensitive to a change in population size than phenotypes maturing at older ages, K‐selection can favor delayed onset of maturation. We analyze a general stochastic Leslie‐matrix model with a simplified density regulation affecting all survivals equally through a function of the population vector, often called the ‘critical age class’. We show that the outcome of such an age‐dependent r‐ and K‐selection is that the expected value of the ‘critical age class’ is maximized by evolution, a strategy strongly influenced by the magnitude of the environmental stochasticity. We also demonstrate that evolution caused by such density‐dependent selection influences the population dynamics, showing a possible reciprocal effect between ecology and evolution in age‐structured populations. This modeling approach reveals that changes in population size affecting the fitness of phenotypes with different age of maturity may be an important selective agent for variation in onset of reproduction in fluctuating environments. This provides a testable hypothesis for how patterns in the population dynamics should affect life history variation.     

On the fate of sexual traits under asexuality

Environmental shifts and life‐history changes may result in formerly adaptive traits becoming non‐functional or maladaptive. In the absence of pleiotropy and other constraints, such traits may decay as a consequence of neutral mutation accumulation or selective processes, highlighting the importance of natural selection for adaptations. A suite of traits are expected to lose their adaptive function in asexual organisms derived from sexual ancestors, and the many independent transitions to asexuality allow for comparative studies of parallel trait maintenance versus decay. In addition, because certain traits, notably male‐specific traits, are usually not exposed to selection under asexuality, their decay would have to occur as a consequence of drift. Selective processes could drive the decay of traits associated with costs, which may be the case for the majority of sexual traits expressed in females. We review the fate of male and female sexual traits in 93 animal lineages characterized by asexual reproduction, covering a broad taxon range including molluscs, arachnids, diplopods, crustaceans and eleven different hexapod orders. Many asexual lineages are still able occasionally to produce males. These asexually produced males are often largely or even fully functional, revealing that major developmental pathways can remain quiescent and functional over extended time periods. By contrast, for asexual females, there is a parallel and rapid decay of sexual traits, especially of traits related to mate attraction and location, as expected given the considerable costs often associated with the expression of these traits. The level of decay of female sexual traits, in addition to asexual females being unable to fertilize their eggs, would severely impede reversals to sexual reproduction, even in recently derived asexual lineages. More generally, the parallel maintenance versus decay of different trait types across diverse asexual lineages suggests that neutral traits display little or no decay even after extended periods under relaxed selection, while extensive decay for selected traits occurs extremely quickly. These patterns also highlight that adaptations can fix rapidly in natural populations of asexual organisms, in spite of their mode of reproduction.     

Evolution of alternative insect life histories in stochastic seasonal environments

Deterministic seasonality can explain the evolution of alternative life history phenotypes (i.e., life history polyphenism) expressed in different generations emerging within the same year. However, the influence of stochastic variation on the expression of such life history polyphenisms in seasonal environments is insufficiently understood. Here, we use insects as a model and explore (1) the effects of stochastic variation in seasonality and (2) the life cycle on the degree of life history differentiation among the alternative developmental pathways of direct development and diapause (overwintering), and (3) the evolution of phenology. With numerical simulation, we determine the values of development (growth) time, growth rate, body size, reproductive effort, adult life span, and fecundity in both the overwintering and directly developing generations that maximize geometric mean fitness. The results suggest that natural selection favors the expression of alternative life histories in the alternative developmental pathways even when there is stochastic variation in seasonality, but that trait differentiation is affected by the developmental stage that overwinters. Increasing environmental unpredictability induced a switch to a bet‐hedging type of life history strategy, which is consistent with general life history theory. Bet‐hedging appeared in our study system as reduced expression of the direct development phenotype, with associated changes in life history phenotypes, because the fitness value of direct development is highly variable in uncertain environments. Our main result is that seasonality itself is a key factor promoting the evolution of seasonally polyphenic life histories but that environmental stochasticity may modulate the expression of life history phenotypes.     

Coalescence 2.0: a multiple branching of recent theoretical developments and their applications

Population genetics theory has laid the foundations for genomic analyses including the recent burst in genome scans for selection and statistical inference of past demographic events in many prokaryote, animal and plant species. Identifying SNPs under natural selection and underpinning species adaptation relies on disentangling the respective contribution of random processes (mutation, drift, migration) from that of selection on nucleotide variability. Most theory and statistical tests have been developed using the Kingman coalescent theory based on the Wright‐Fisher population model. However, these theoretical models rely on biological and life history assumptions which may be violated in many prokaryote, fungal, animal or plant species. Recent theoretical developments of the so‐called multiple merger coalescent models are reviewed here (Λ‐coalescent, beta‐coalescent, Bolthausen‐Sznitman, Ξ‐coalescent). We explain how these new models take into account various pervasive ecological and biological characteristics, life history traits or life cycles which were not accounted in previous theories such as (i) the skew in offspring production typical of marine species, (ii) fast adapting microparasites (virus, bacteria and fungi) exhibiting large variation in population sizes during epidemics, (iii) the peculiar life cycles of fungi and bacteria alternating sexual and asexual cycles and (iv) the high rates of extinction‐recolonization in spatially structured populations. We finally discuss the relevance of multiple merger models for the detection of SNPs under selection in these species, for population genomics of very large sample size and advocate to potentially examine the conclusion of previous population genetics studies.     

Convergent transformation and selection in cultural evolution

In biology, natural selection is the main explanation of adaptations and it is an attractive idea to think that an analogous force could have the same role in cultural evolution. In support of this idea, all the main ingredients for natural selection have been documented in the cultural domain. However, the changes that occur during cultural transmission typically result in convergent transformation, non-random cultural modifications, casting some doubts on the importance of natural selection in the cultural domain. To progress on this issue more empirical research is needed. Here, using nearly half a million experimental trials performed by a group of baboons (Papio papio), we simulate cultural evolution under various conditions of natural selection and do an additional experiment to tease apart the role of convergent transformation and selection. Our results confirm that transformation strongly constrain the variation available to selection and therefore strongly limit its impact on cultural evolution. Surprisingly, in our study, transformation also enhances the effect of selection by stabilising cultural variation. We conclude that, in culture, selection can change the evolutionary trajectory substantially in some cases, but can only act on the variation provided by (typically biased) transformation.     

Genus-Wide Characterization of Bumblebee Genomes Provides Insights into Their Evolution and Variation in Ecological and Behavioral Traits

Bumblebees are a diverse group of globally important pollinators in natural ecosystems and for agricultural food production. With both eusocial and solitary life-cycle phases, and some social parasite species, they are especially interesting models to understand social evolution, behavior, and ecology. Reports of many species in decline point to pathogen transmission, habitat loss, pesticide usage, and global climate change, as interconnected causes. These threats to bumblebee diversity make our reliance on a handful of well-studied species for agricultural pollination particularly precarious. To broadly sample bumblebee genomic and phenotypic diversity, we de novo sequenced and assembled the genomes of 17 species, representing all 15 subgenera, producing the first genus-wide quantification of genetic and genomic variation potentially underlying key ecological and behavioral traits. The species phylogeny resolves subgenera relationships, whereas incomplete lineage sorting likely drives high levels of gene tree discordance. Five chromosome-level assemblies show a stable 18-chromosome karyotype, with major rearrangements creating 25 chromosomes in social parasites. Differential transposable element activity drives changes in genome sizes, with putative domestications of repetitive sequences influencing gene coding and regulatory potential. Dynamically evolving gene families and signatures of positive selection point to genus-wide variation in processes linked to foraging, diet and metabolism, immunity and detoxification, as well as adaptations for life at high altitudes. Our study reveals how bumblebee genes and genomes have evolved across the Bombus phylogeny and identifies variations potentially linked to key ecological and behavioral traits of these important pollinators.     

Multimodal signals in male European treefrog (Hyla arborea) and the influence of population isolation on signal expression

In nocturnal treefrogs, mate choice implies the use of acoustic and visual signals. Multimodality is suspected to have evolved for either information redundancy or information complementariness. It is essential to explore multimodality in a natural context to understand the selection pressures operating on the signals. In the present study, we investigated calling and coloration in relation to male biometry and condition in four populations of European treefrog (Hyla arborea) varying in size and genetic isolation. We compared the signal intensity between core and satellite populations to estimate the impact of genetic diversity on male secondary sexual traits. The results obtained show important regional variations in both traits, likely as a result of local adaptations. Call and coloration are weakly correlated within an individual, implying that these traits likely convey different information about the signaller's identity or quality, thus supporting the hypothesis of complementariness of multiple messages. By contrast to the experimental evidence, we find that call and coloration are not related to male condition (as estimated by the residual of mass over size), suggesting that the condition‐dependence of these traits may be mediated by complex mechanisms not accurately reflected by the chosen estimator. Finally, male call and colour phenotypes present no robust pattern of variation with isolation status, probably because of variation in local selective pressures and in history of population dynamics. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 633–647.     

The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence

There is large spatial and temporal variation in the Gyrodactylus parasite fauna across natural guppy (Poecilia reticulata) populations in Trinidad. The life history evolution of these fish could be affected differently in the various habitats depending on the local parasite selection pressure. Here, we experimentally infected three guppy populations with three gyrodactylid strains in the laboratory and monitored the infection by recording the number of parasites and host mortality in a full factorial design. The origin of the guppy population and parasite strain, and the size of the hosts explained significant variation in the survival of hosts. Larger fish carried the highest parasite loads and experienced the highest mortality rates, which suggests that parasite-mediated selection may favour smaller phenotypes, possibly counter-balancing selection pressures by gape-limited predators, mate choice and female fecundity. We observed significant variation in virulence between parasite strains with the captive-bred experimental strain (Gt3) causing the highest mortality of hosts whilst reaching only relatively low maximum burdens. This suggests that adaptations to the captive environment and/or inbreeding depression may alter the virulence of such captive-bred parasites. There were significant differences in survival rate between guppy populations, with infected guppies from the large population of the Lower Aripo River showing a higher survival rate than the fish from the small and genetically less diverse Upper Aripo River population.     

Accelerated discovery of functional genomic variation in pigs

The genotype-phenotype link is a major research topic in the life sciences but remains highly complex to disentangle. Part of the complexity arises from the number of genes contributing to the observed phenotype. Despite the vast increase of molecular data, pinpointing the causal variant underlying a phenotype of interest is still challenging. In this study, we present an approach to map causal variation and molecular pathways underlying important phenotypes in pigs. We prioritize variation by utilizing and integrating predicted variant impact scores (pCADD), functional genomic information, and associated phenotypes in other mammalian species. We demonstrate the efficacy of our approach by reporting known and novel causal variants, of which many affect non-coding sequences. Our approach allows the disentangling of the biology behind important phenotypes by accelerating the discovery of novel causal variants and molecular mechanisms affecting important phenotypes in pigs. This information on molecular mechanisms could be applicable in other mammalian species, including humans.     

Colonisation of toxic environments drives predictable life‐history evolution in livebearing fishes (Poeciliidae)

New World livebearing fishes (family Poeciliidae) have repeatedly colonised toxic, hydrogen sulphide‐rich waters across their natural distribution. Physiological considerations and life‐history theory predict that these adverse conditions should favour the evolution of larger offspring. Here, we examined nine poeciliid species that independently colonised toxic environments, and show that these fishes have indeed repeatedly evolved much larger offspring size at birth in sulphidic waters, thus uncovering a widespread pattern of predictable evolution. However, a second pattern, only indirectly predicted by theory, proved additionally common: a reduction in the number of offspring carried per clutch (i.e. lower fecundity). Our analyses reveal that this secondary pattern represents a mere consequence of a classic life‐history trade‐off combined with strong selection on offspring size alone. With such strong natural selection in extreme environments, extremophile organisms may commonly exhibit multivariate phenotypic shifts even though not all diverging traits necessarily represent adaptations to the extreme conditions.