Parasite load, rather than parasite presence, decreases upstream movement in Trinidadian guppies Poecilia reticulata.

Several factors influence whether an organism remains in its local habitat. Parasites can, for example, influence host movement by impacting their behavior, physiology, and morphology. In rivers, fish that swim efficiently against the current are able to maintain their position without being displaced downstream, a behavior referred to as positive rheotaxis. We hypothesized that both the presence and number of ectoparasites on a host would affect the ability of fish to avoid downstream displacement and thus prevent them from remaining in their habitat. We used the guppy-Gyrodactylus host-ectoparasite model to test whether parasite presence and parasite load had an effect on fish rheotaxis. We quantified rheotaxis of sham-infected and parasite-infected fish in a circular flow tank in the laboratory prior to infection and 5-6 days postinfection. Both parasite-infected and sham-infected individuals expressed similar levels of positive rheotaxis prior to infection and after infection. However, with increasing parasite numbers, guppies covered less distance in the upstream direction and spent more time in slower flow zones. These results suggest that higher numbers of Gyrodactylus ectoparasites negatively influence rheotactic movements. Further research is needed to understand the ecological and evolutionary implications of this ectoparasite on fish movement.

Recent declines in salmon body size impact ecosystems and fisheries.

Declines in animal body sizes are widely reported and likely impact ecological interactions and ecosystem services. For harvested species subject to multiple stressors, limited understanding of the causes and consequences of size declines impedes prediction, prevention, and mitigation. We highlight widespread declines in Pacific salmon size based on 60 years of measurements from 12.5 million fish across Alaska, the last largely pristine North American salmon-producing region. Declines in salmon size, primarily resulting from shifting age structure, are associated with climate and competition at sea. Compared to salmon maturing before 1990, the reduced size of adult salmon after 2010 has potentially resulted in substantial losses to ecosystems and people; for Chinook salmon we estimated average per-fish reductions in egg production (-16%), nutrient transport (-28%), fisheries value (-21%), and meals for rural people (-26%). Downsizing of organisms is a global concern, and current trends may pose substantial risks for nature and people.

Melanin-based coloration and host-parasite interactions under global change.

The role of parasites in shaping melanin-based colour polymorphism, and the consequences of colour polymorphism for disease resistance, remain debated. Here we review recent evidence of the links between melanin-based coloration and the behavioural and immunological defences of vertebrates against their parasites. First we propose that (1) differences between colour morphs can result in variable exposure to parasites, either directly (certain colours might be more or less attractive to parasites) or indirectly (variations in behaviour and encounter probability). Once infected, we propose that (2) immune variation between differently coloured individuals might result in different abilities to cope with parasite infection. We then discuss (3) how these different abilities could translate into variable sexual and natural selection in environments varying in parasite pressure. Finally, we address (4) the potential role of parasites in the maintenance of melanin-based colour polymorphism, especially in the context of global change and multiple stressors in human-altered environments. Because global change will probably affect both coloration and the spread of parasitic diseases in the decades to come, future studies should take into account melanin-based coloration to better predict the evolutionary responses of animals to changing disease risk in human-altered environments.

Heritable gene expression differences between lake and stream stickleback include both parallel and antiparallel components.

The repeated phenotypic patterns that characterize populations undergoing parallel evolution provide support for a deterministic role of adaptation by natural selection. Determining the level of parallelism also at the genetic level is thus central to our understanding of how natural selection works. Many studies have looked for repeated genomic patterns in natural populations, but work on gene expression is less common. The studies that have examined gene expression have found some support for parallelism, but those studies almost always used samples collected from the wild that potentially confounds the effects of plasticity with heritable differences. Here we use two independent pairs of lake and stream threespine stickleback (Gasterosteus aculeatus) raised in common garden conditions to assess both parallel and antiparallel (that is, similar versus different directions of lake-stream expression divergence in the two watersheds) heritable gene expression differences as measured by total RNA sequencing. We find that more genes than expected by chance show either parallel (22 genes, 0.18% of expressed genes) or antiparallel (24 genes, 0.20% of expressed genes) lake-stream expression differences. These results correspond well with previous genomic studies in stickleback ecotype pairs that found similar levels of parallelism. We suggest that parallelism might be similarly constrained at the genomic and transcriptomic levels.

Evolutionary and immediate effects of crude-oil pollution: depression of exploratory behaviour across populations of Trinidadian guppies.

Human-induced perturbations such as crude-oil pollution can pose serious threats to aquatic ecosystems. To understand these threats fully it is important to establish both the immediate and evolutionary effects of pollutants on behaviour and cognition. Addressing such questions requires comparative and experimental study of populations that have evolved under different levels of pollution. Here, we compared the exploratory, activity and social behaviour of four populations of Trinidadian guppies (Poecilia reticulata) raised in common garden conditions for up to three generations. Two of these populations originated from tributaries with a long history of human-induced chronic crude-oil pollution with polycyclic aromatic hydrocarbons due to oil exploitation in Trinidad, the two others originating from non-polluted control sites. Laboratory-raised guppies from the oil-polluted sites were less exploratory in an experimental maze than guppies from the non-polluted sites and in a similar manner for the two independent rivers. We then compared the plastic behavioural responses of the different populations after an acute short-term experimental exposure to crude oil and found a decrease in exploration (but not in activity or shoaling) in the oil-exposed fish compared to the control subjects over all four populations. Taken together, these results suggest that both an evolutionary history with oil and an acute exposure to oil depressed guppy exploratory behaviour. We discuss whether the behavioural divergence observed represents adaptation to human-induced pollutants, the implications for conservation and the possible knock-on effects for information discovery and population persistence in fish groups.

Improving the forecast for biodiversity under climate change.

New biological models are incorporating the realistic processes underlying biological responses to climate change and other human-caused disturbances. However, these more realistic models require detailed information, which is lacking for most species on Earth. Current monitoring efforts mainly document changes in biodiversity, rather than collecting the mechanistic data needed to predict future changes. We describe and prioritize the biological information needed to inform more realistic projections of species' responses to climate change. We also highlight how trait-based approaches and adaptive modeling can leverage sparse data to make broader predictions. We outline a global effort to collect the data necessary to better understand, anticipate, and reduce the damaging effects of climate change on biodiversity.

Assessing reproductive isolation using a contact zone between parapatric lake-stream stickleback ecotypes.

Ecological speciation occurs when populations evolve reproductive isolation as a result of divergent natural selection. This isolation can be influenced by many potential reproductive barriers, including selection against hybrids, selection against migrants and assortative mating. How and when these barriers act and interact in nature is understood for relatively few empirical systems. We used a mark-recapture experiment in a contact zone between lake and stream three-spined sticklebacks (Gasterosteus aculeatus, Linnaeus) to evaluate the occurrence of hybrids (allowing inferences about mating isolation), the interannual survival of hybrids (allowing inferences about selection against hybrids) and the shift in lake-like vs. stream-like characteristics (allowing inferences about selection against migrants). Genetic and morphological data suggest the occurrence of hybrids and no selection against hybrids in general, a result contradictory to a number of other studies of sticklebacks. However, we did find selection against more lake-like individuals, suggesting a barrier to gene flow from the lake into the stream. Combined with previous work on this system, our results suggest that multiple (most weakly and often asymmetric) barriers must be combining to yield substantial restrictions on gene flow. This work provides evidence of a reproductive barrier in lake-stream sticklebacks and highlights the value of assessing multiple reproductive barriers in natural contexts.

The context dependence of assortative mating: a demonstration with conspecific salmonid populations.

Assortative mating is thought to play a key role in reproductive isolation. However, most experimental studies of assortative mating do not take place in multiple natural environments, and hence, they ignore its potential context dependence. We implemented an experiment in which two populations of brown trout (Salmo trutta) with different natural flow regimes were placed into semi-natural stream channels under two different artificial flow regimes. Natural reproduction was allowed, and reproductive isolation was measured by means of parentage assignment to compare within-population vs. between-population male-female mating and relative offspring production. For both metrics, reproductive isolation was highly context dependent: no isolation was evident under one flow regime, but strong isolation was evident under the other flow regime. These patterns were fully driven by variance in the mating success of males from one of the two populations. Our results highlight how reproductive isolation through assortative mating can be strongly context dependent, which could have dramatic consequences for patterns of gene flow and speciation under environmental change.

Parallel and nonparallel behavioural evolution in response to parasitism and predation in Trinidadian guppies.

Natural enemies such as predators and parasites are known to shape intraspecific variability of behaviour and personality in natural populations, yet several key questions remain: (i) What is the relative importance of predation vs. parasitism in shaping intraspecific variation of behaviour across generations? (ii) What are the contributions of genetic and plastic effects to this behavioural divergence? (iii) And to what extent are responses to predation and parasitism repeatable across independent evolutionary lineages? We addressed these questions using Trinidadian guppies (Poecilia reticulata) (i) varying in their exposure to dangerous fish predators and Gyrodactylus ectoparasites for (ii) both wild-caught F0 and laboratory-reared F2 individuals and coming from (iii) multiple independent evolutionary lineages (i.e. independent drainages). Several key findings emerged. First, a population's history of predation and parasitism influenced behavioural profiles, but to different extent depending on the behaviour considered (activity, shoaling or boldness). Second, we had evidence for some genetic effects of predation regime on behaviour, with differences in activity of F2 laboratory-reared individuals, but not for parasitism, which had only plastic effects on the boldness of wild-caught F0 individuals. Third, the two lineages showed a mixture of parallel and nonparallel responses to predation/parasitism, with parallel responses being stronger for predation than for parasitism and for activity and boldness than for shoaling. These findings suggest that different sets of behaviours provide different pay-offs in alternative predation/parasitism environments and that parasitism has more transient effects in shaping intraspecific variation of behaviour than does predation.

Parting ways: parasite release in nature leads to sex-specific evolution of defence.

We evaluated the extent to which males and females evolve along similar or different trajectories in response to the same environmental shift. Specifically, we used replicate experimental introductions in nature to consider how release from a key parasite (Gyrodactylus) generates similar or different defence evolution in male vs. female guppies (Poecilia reticulata). After 4-8 generations of evolution, guppies were collected from the ancestral (parasite still present) and derived (parasite now absent) populations and bred for two generations in the laboratory to control for nongenetic effects. These F2 guppies were then individually infected with Gyrodactylus, and infection dynamics were monitored on each fish. We found that parasite release in nature led to sex-specific evolutionary responses: males did not show much evolution of resistance, whereas females showed the evolution of increased resistance. Given that male guppies in the ancestral population had greater resistance to Gyrodactylus than did females, evolution in the derived populations led to reduction of sexual dimorphism in resistance. We argue that previous selection for high resistance in males constrained (relative to females) further evolution of the trait. We advocate more experiments considering sex-specific evolutionary responses to environmental change.

Does plasticity enhance or dampen phenotypic parallelism? A test with three lake-stream stickleback pairs.

Parallel (and convergent) phenotypic variation is most often studied in the wild, where it is difficult to disentangle genetic vs. environmentally induced effects. As a result, the potential contributions of phenotypic plasticity to parallelism (and nonparallelism) are rarely evaluated in a formal sense. Phenotypic parallelism could be enhanced by plasticity that causes stronger parallelism across populations in the wild than would be expected from genetic differences alone. Phenotypic parallelism could be dampened if site-specific plasticity induced differences between otherwise genetically parallel populations. We used a common-garden study of three independent lake-stream stickleback population pairs to evaluate the extent to which adaptive divergence has a genetic or plastic basis, and to investigate the enhancing vs. dampening effects of plasticity on phenotypic parallelism. We found that lake-stream differences in most traits had a genetic basis, but that several traits also showed contributions from plasticity. Moreover, plasticity was much more prevalent in one watershed than in the other two. In most cases, plasticity enhanced phenotypic parallelism, whereas in a few cases, plasticity had a dampening effect. Genetic and plastic contributions to divergence seem to play a complimentary, likely adaptive, role in phenotypic parallelism of lake-stream stickleback. These findings highlight the value of formally comparing wild-caught and laboratory-reared individuals in the study of phenotypic parallelism.

Testing for parallel allochronic isolation in lake-stream stickleback.

The evolution of reproductive isolation (RI) is a critical step shaping progress towards speciation. In the context of ecological speciation, a critical question is the extent to which specific reproductive barriers important to RI evolve rapidly and predictably in response to environmental differences. Only reproductive barriers with these properties (importance, rapidity, predictability) will drive the diversification of species that are cohesively structured by environment type. One candidate barrier that might exhibit such properties is allochrony, whereby populations breed at different times. We studied six independent lake-stream population pairs of threespine stickleback (Gasterosteus aculeatus Linnaeus, 1758) that are known from genetic studies to show RI. However, the specific reproductive barriers driving this RI have proven elusive, leading to a 'conundrum of missing reproductive isolation'. We here show that breeding times differ among some of the populations, but not in a consistent manner between lakes and streams. Moreover, the timing differences between lake and stream populations within each pair could account for only a small proportion of total RI measured with neutral genetic markers. Allochrony cannot solve the conundrum of missing reproductive isolation in lake-stream stickleback.

Darwin's finches and their diet niches: the sympatric coexistence of imperfect generalists.

Adaptive radiation can be strongly influenced by interspecific competition for resources, which can lead to diverse outcomes ranging from competitive exclusion to character displacement. In each case, sympatric species are expected to evolve into distinct ecological niches, such as different food types, yet this expectation is not always met when such species are examined in nature. The most common hypotheses to account for the coexistence of species with substantial diet overlap rest on temporal variation in niches (often diets). Yet spatial variation in niche overlap might also be important, pointing to the need for spatiotemporal analyses of diet and diet overlap between closely related species persisting in sympatry. We here perform such an analysis by characterizing the diets of, and diet overlap among, four sympatric Darwin's ground finch species at three sites and over 5 years on a single Galápagos island (Santa Cruz). We find that the different species have broadly similar and overlapping diets - they are to some extent generalists and opportunists - yet we also find that each species retains some 'private' resources for which their morphologies are best suited. Importantly, use of these private resources increased considerably, and diet overlap decreased accordingly, when the availability of preferred shared foods, such as arthropods, was reduced during drought conditions. Spatial variation in food resources was also important. These results together suggest that the ground finches are 'imperfect generalists' that use overlapping resources under benign conditions (in space or time), but then retreat to resources for which they are best adapted during periods of food limitation. These conditions likely promote local and regional coexistence.

Key questions in the genetics and genomics of eco-evolutionary dynamics.

Increasing acceptance that evolution can be 'rapid' (or 'contemporary') has generated growing interest in the consequences for ecology. The genetics and genomics of these 'eco-evolutionary dynamics' will be--to a large extent--the genetics and genomics of organismal phenotypes. In the hope of stimulating research in this area, I review empirical data from natural populations and draw the following conclusions. (1) Considerable additive genetic variance is present for most traits in most populations. (2) Trait correlations do not consistently oppose selection. (3) Adaptive differences between populations often involve dominance and epistasis. (4) Most adaptation is the result of genes of small-to-modest effect, although (5) some genes certainly have larger effects than the others. (6) Adaptation by independent lineages to similar environments is mostly driven by different alleles/genes. (7) Adaptation to new environments is mostly driven by standing genetic variation, although new mutations can be important in some instances. (8) Adaptation is driven by both structural and regulatory genetic variation, with recent studies emphasizing the latter. (9) The ecological effects of organisms, considered as extended phenotypes, are often heritable. Overall, the study of eco-evolutionary dynamics will benefit from perspectives and approaches that emphasize standing genetic variation in many genes of small-to-modest effect acting across multiple traits and that analyze overall adaptation or 'fitness'. In addition, increasing attention should be paid to dominance, epistasis and regulatory variation.

Environmental factors influencing adult sex ratio in Poecilia reticulata: laboratory experiments.

The potential causes of adult sex ratio variation in guppies Poecilia reticulata were tested in laboratory experiments that evaluated the mortality rates of male and female P. reticulata exposed to potential predators (Hart's rivulus Rivulus hartii and freshwater prawns Macrobrachium crenulatum) and to different resource levels. Poecilia reticulata mortality increased in the presence of R. hartii and M. crenulatum, and low resource levels had an effect on mortality only in the presence of M. crenulatum. Rivulus hartii preyed more often on male than on female P. reticulata, and this sex-biased predation was not simply the result of males being smaller than females. In contrast, no sex-biased mortality was attributable to M. crenulatum or low resource levels.

Factors influencing progress toward sympatric speciation.

Many factors could influence progress towards sympatric speciation. Some of the potentially important ones include competition, mate choice and the degree to which alternative sympatric environments (resources) are discrete. What is not well understood is the relative importance of these different factors, as well as interactions among them. We use an individual-based numerical model to investigate the possibilities. Mate choice was modelled as the degree to which male foraging traits influence female mate choice. Competition was modelled as the degree to which individuals with different phenotypes compete for portions of the resource distribution. Discreteness of the environment was modelled as the degree of bimodality of the underlying resource distribution. We find that strong mate choice was necessary, but not sufficient, to cause sympatric speciation. In addition, sympatric speciation was most likely when the resource distribution was strongly bimodal and when competition among different phenotypes was intermediate. Even under these ideal conditions, however, sympatric speciation occurred only a fraction of the time. Sympatric speciation owing to competition on unimodal resource distributions was also possible, but much less common. In all cases, stochasticity played an important role in determining progress towards sympatric speciation, as evidenced by variation in outcomes among replicate simulations for a given set of parameter values. Overall, we conclude that the nature of competition is much less important for sympatric speciation than is the nature of mate choice and the underlying resource distribution. We argue that an increased understanding of the promoters and inhibitors of sympatric speciation is best achieved through models that simultaneously evaluate multiple potential factors.

Quantitative genetic inheritance of morphological divergence in a lake-stream stickleback ecotype pair: implications for reproductive isolation.

Ecological selection against hybrids between populations occupying different habitats might be an important component of reproductive isolation during the initial stages of speciation. The strength and directionality of this barrier to gene flow depends on the genetic architecture underlying divergence in ecologically relevant phenotypes. We here present line cross analyses of inheritance for two key foraging-related morphological traits involved in adaptive divergence between stickleback ecotypes residing parapatrically in lake and stream habitats within the Misty Lake watershed (Vancouver Island, Canada). One main finding is the striking genetic dominance of the lake phenotype for body depth. Selection associated with this phenotype against first- and later-generation hybrids should therefore be asymmetric, hindering introgression from the lake to the stream population but not vice versa. Another main finding is that divergence in gill raker number is inherited additively and should therefore contribute symmetrically to reproductive isolation. Our study suggests that traits involved in adaptation might contribute to reproductive isolation qualitatively differently, depending on their mode of inheritance.

Eco-evolutionary dynamics in Pacific salmon.

Increasing acceptance of the idea that evolution can proceed rapidly has generated considerable interest in understanding the consequences of ongoing evolutionary change for populations, communities and ecosystems. The nascent field of 'eco-evolutionary dynamics' considers these interactions, including reciprocal feedbacks between evolution and ecology. Empirical support for eco-evolutionary dynamics has emerged from several model systems, and we here present some possibilities for diverse and strong effects in Pacific salmon (Oncorhynchus spp.). We specifically focus on the consequences that natural selection on body size can have for salmon population dynamics, community (bear-salmon) interactions and ecosystem process (fluxes of salmon biomass between habitats). For example, we find that shifts in body size because of selection can alter fluxes across habitats by up to 11% compared with ecological (that is, numerical) effects. More generally, we show that selection within a generation can have large effects on ecological dynamics and so should be included within a complete eco-evolutionary framework.

Genetic divergence in morphology-performance mapping between Misty Lake and inlet stickleback.

Different environments should select for different aspects of organismal performance, which should lead to correlated divergence in morphological traits that influence performance. The result should be genetic divergence in aspects of performance, morphology and associations ('maps') between morphology and performance. Testing this hypothesis requires quantifying performance and morphology in multiple populations after controlling for environmental differences, but this is rarely attempted. We used a common-garden experiment to examine morphology and several aspects of swimming performance within and between the lake and inlet populations of threespine stickleback (Gasterosteus aculeatus) from the Misty system, Vancouver Island, Canada. Controlling for body size, lake stickleback had shallower bodies, larger caudal fins and smaller pelvic girdles. With or without morphological covariates, lake stickleback showed greater performance in both sustained and burst swimming. In contrast, inlet stickleback showed greater manoeuverability than did lake stickleback in some analyses. Morphology-performance relationships were decoupled when considering variation within vs. between populations. Moreover, morphology-performance mapping differed between the two populations. Based on these observations, we advance a hypothesis for why populations adapting to different environments should show adaptive genetic divergence in morphology-performance mapping.

The consequences of phenotypic plasticity for ecological speciation.

We use an individual-based numerical simulation to study the effects of phenotypic plasticity on ecological speciation. We find that adaptive plasticity evolves readily in the presence of dispersal between populations from different ecological environments. This plasticity promotes the colonization of new environments but reduces genetic divergence between them. We also find that the evolution of plasticity can either enhance or degrade the potential for divergent selection to form reproductive barriers. Of particular importance here is the timing of plasticity in relation to the timing of dispersal. If plasticity is expressed after dispersal, reproductive barriers are generally weaker because plasticity allows migrants to be better suited for their new environment. If plasticity is expressed before dispersal, reproductive barriers are either unaffected or enhanced. Among the potential reproductive barriers we considered, natural selection against migrants was the most important, primarily because it was the earliest-acting barrier. Accordingly, plasticity had a much greater effect on natural selection against migrants than on sexual selection against migrants or on natural and sexual selection against hybrids. In general, phenotypic plasticity can strongly alter the process of ecological speciation and should be considered when studying the evolution of reproductive barriers.