Evolution in heterogeneous environments: Effects of migration on habitat specialization

Summary Richard Levins introduced fitness sets as a tool for investigating evolution within heterogeneous environments. Evolutionary game theory permits a synthesis and generalization of this approach by considering the evolutionary response of organisms to any scale of habitat heterogeneity. As scales of heterogeneity increase from fine to coarse, the evolutionary stable strategy (ESS) switches from a single generalist species to several species that become increasingly specialized on distinct habitats. Depending upon the organisms' ecology, the switch from one to two species may occur at high migration rates (relatively fine-grained environment), or may only occur at very low migration rates (coarse-grained environment). At the ESS, the evolutionary context of a species is the entire landscape, while its ecological context may be a single habitat.Evolution towards the ESS can be represented with adaptive landscapes. In the absence of frequency-dependence, shifting from a single strategy ESS to a two strategy ESS poses the problem of evolving across valleys in the adaptive surface to occupy new peaks (hence, Sewell Wright's shifting balance theory). Frequency-dependent processes facilitate evolution across valleys. If a system with a two strategy ESS is constrained to possess a single strategy, the population may actually evolve a strategy that minimizes fitness. Because the population now rests at the bottom of a valley, evolution by natural selection can drive populations to occupy both peaks.     

Rebound in functional distinctiveness following warming and reduced fishing in the North Sea

Functionally distinct species (i.e. species with unique trait combinations in the community) can support important ecological roles and contribute disproportionately to ecosystem functioning. Yet, how functionally distinct species have responded to recent climate change and human exploitation has been widely overlooked. Here, using ecological traits and long-term fish data in the North Sea, we identified functionally distinct and functionally common species, and evaluated their spatial and temporal dynamics in relation to environmental variables and fishing pressure. Functionally distinct species were characterized by late sexual maturity, few, large offspring, and high parental care, many being sharks and skates that play critical roles in structuring food webs. Both functionally distinct and functionally common species increased in abundance as ocean temperatures warmed and fishing pressure decreased over the last three decades; however, functionally distinct species increased throughout the North Sea, but primarily in southern North Sea where fishing was historically most intense, indicating a rebound following fleet decommissioning and reduced harvesting. Yet, some of the most functionally distinct species are currently listed as threatened by the IUCN and considered highly vulnerable to fishing pressure. Alarmingly these species have not rebounded. This work highlights the relevance and potential of integrating functional distinctiveness into ecosystem management and conservation prioritization.     

Links to rare climates do not translate into distinct traits for island endemics

Current models of island biogeography treat endemic and non-endemic species as if they were functionally equivalent, focussing primarily on species richness. Thus, the functional composition of island biotas in relation to island biogeographical variables remains largely unknown. Using plant trait data (plant height, leaf area and flower length) for 895 native species in the Canary Islands, we related functional trait distinctiveness and climate rarity for endemic and non-endemic species and island ages. Endemics showed a link to climatically rare conditions that is consistent with island geological change through time. However, functional trait distinctiveness did not differ between endemics and non-endemics and remained constant with island age. Thus, there is no obvious link between trait distinctiveness and occupancy of rare climates, at least for the traits measured here, suggesting that treating endemic and non-endemic species as functionally equivalent in island biogeography is not fundamentally wrong.     

Functional trait differences influence neighbourhood interactions in a hyperdiverse Amazonian forest

As distinct community assembly processes can produce similar community patterns, assessing the ecological mechanisms promoting coexistence in hyperdiverse rainforests remains a considerable challenge. We use spatially explicit neighbourhood models of tree growth to quantify how functional trait and phylogenetic similarities predict variation in growth and crowding effects for the 315 most abundant tree species in a 25‐ha lowland rainforest plot in Ecuador. We find that functional trait differences reflect variation in (1) species maximum potential growth, (2) the intensity of interspecific interactions for some species, and (3) species sensitivity to neighbours. We find that neighbours influenced tree growth in 28% of the 315 focal tree species. Neighbourhood effects are not detected in the remaining 72%, which may reflect the low statistical power to model rare taxa and/or species insensitivity to neighbours. Our results highlight the spectrum of ways in which functional trait differences can shape community dynamics in highly diverse rainforests.     

High evolutionary and functional distinctiveness of endemic monocots in world islands

Functionally and evolutionarily distinct species have traits or an evolutionary history that are shared by few others in a given set, which make them priority species for biodiversity conservation. On islands, life in isolation has led to the evolution of many distinct forms and functions as well as to a high level of endemism. The aim of this study is to assess the evolutionary and functional distinctiveness of insular monocotyledons and their distribution across 126 islands worldwide. We show that evolutionary and functional distinctiveness are decoupled but that both are higher on islands than on continental areas. Anagenesis on islands followed by extinctions and/or diversification on the mainland may have led to highly evolutionarily distinct species while functionally distinct species may have arisen from ecological niche shift or niche expansion. Insular endemic species with high evolutionary distinctiveness but not with high functional distinctiveness are significantly range-restricted compared to less distinct species, possibly indicating differences in dispersal potential. By showing that distinctiveness is high on islands and that the most distinct species are range-restricted, our study has important conservation implications. Indeed, islands are among the most threatened systems of the world, and extinctions of the most distinct species could lead to significant loss of phylogenetic and functional diversity.

     

Habitat heterogeneity promotes intraspecific trait variability of shrub species in Australian granite inselbergs

The role of intraspecific trait variability is increasingly recognized as a key factor shaping plant fitness and community assembly worldwide. Studying the direct effects of habitat heterogeneity on trait expression of individual plants of the same species is a useful tool to quantify intraspecific trait variability locally. We investigated how habitat heterogeneity on granite inselbergs affected intraspecific trait variability of 19 functional traits in three shrub species of the family Proteaceae in south western Australia, a global biodiversity hotspot. We used pairwise comparison (single trait) and multivariate analysis (multiple traits, functional space) to detect shifts in trait patterns. Consistent with our predictions, we found that individuals developing in putatively more stressful habitats (highly sun-irradiated, shallow-soil patches on the outcrops) were characterized by trait expressions indicative of more conservative resource-related strategies when compared with plants occurring in the surrounding woodlands that were experiencing more benign ecological conditions. These results were significant for two out of three species. Granite inselbergs promoted plant longevity, a signal that these granite inselbergs might offer refugial conditions defined as protection against fire.     

Microfragmentation concept explains non-positive environmental heterogeneity–diversity relationships

Although recent studies have revealed that the relationship between diversity and environmental heterogeneity is not always positive, as classical niche theory predicts, scientists have had difficulty interpreting these results from an ecological perspective. We propose a new concept—microfragmentation—to explain how small-scale heterogeneity can have neutral or even negative effect on species diversity. We define microfragmentation as a community level process of splitting habitat into a more heterogeneous environment that can have non-positive effects on the diversity through habitat loss and subsequent isolation. We provide support for the microfragmentation concept with results from spatially explicit heterogeneity–diversity model simulations, in which varying sets of species (with different ratios of specialist and generalist species) were modeled at different levels of configurational heterogeneity (meaning that only the habitat structure was changed, not its composition). Our results indicate that environmental heterogeneity can affect community diversity in the same way as fragmentation at the landscape level. Although generalist species might not be seriously affected by microfragmentation, the persistence of specialist species can be seriously disturbed by small-scale patchiness. The microfragmentation concept provides new insight into community level diversity dynamics and can influence conservation and management strategies.     

More rich means more diverse: Extending the ‘environmental heterogeneity hypothesis’ to taxonomic diversity

It is widely appreciated that increasing environmental heterogeneity is one of the chief determinants of high species richness. An additional outcome that arises from the relationship between environmental heterogeneity and species richness is that species richer areas are usually taxonomically more diverse than species poor areas. For instance, due to the larger niche availability, species that coexist in heterogeneous environments experience a less severe effect of clustering in their functional traits giving rise to assemblages that are more functionally diverse than in more homogeneous areas. On the other hand, due to the conservatism of many species traits during evolutionary change, the ability of species to colonize the same ecological space is thought to depend at least partially on their taxonomic similarity, such that a positive relationship between the species taxonomic relatedness and their trait similarity is expected. In this paper, we tested the relationship between species richness and taxonomic diversity with 11 florae collected in Latium (Central Italy). The significance of the observed association was then verified with a null model assuming a random distribution of species across the landscape.     

Context dependence in complex adaptive landscapes: frequency and trait‐dependent selection surfaces within an adaptive radiation of Caribbean pupfishes

The adaptive landscape provides the foundational bridge between micro‐ and macroevolution. One well‐known caveat to this perspective is that fitness surfaces depend on ecological context, including competitor frequency, traits measured, and resource abundance. However, this view is based largely on intraspecific studies. It is still unknown how context‐dependence affects the larger features of peaks and valleys on the landscape which ultimately drive speciation and adaptive radiation. Here, I explore this question using one of the most complex fitness landscapes measured in the wild in a sympatric pupfish radiation endemic to San Salvador Island, Bahamas by tracking survival and growth of laboratory‐reared F2 hybrids. I present new analyses of the effects of competitor frequency, dietary isotopes, and trait subsets on this fitness landscape. Contrary to expectations, decreasing competitor frequency increased survival only among very common phenotypes, whereas less common phenotypes rarely survived despite few competitors, suggesting that performance, not competitor frequency, shapes large‐scale features of the fitness landscape. Dietary isotopes were weakly correlated with phenotype and growth, but did not explain additional survival variation. Nonlinear fitness surfaces varied substantially among trait subsets, revealing one‐, two‐, and three‐peak landscapes, demonstrating the complexity of selection in the wild, even among similar functional traits.     

Possible human impacts on adaptive radiation: beak size bimodality in Darwin's finches

Adaptive radiation is facilitated by a rugged adaptive landscape, where fitness peaks correspond to trait values that enhance the use of distinct resources. Different species are thought to occupy the different peaks, with hybrids falling into low-fitness valleys between them. We hypothesize that human activities can smooth adaptive landscapes, increase hybrid fitness and hamper evolutionary diversification. We investigated this possibility by analysing beak size data for 1755 Geospiza fortis measured between 1964 and 2005 on the island of Santa Cruz, Galápagos. Some populations of this species can display a resource-based bimodality in beak size, which mirrors the greater beak size differences among species. We first show that an historically bimodal population at one site, Academy Bay, has lost this property in concert with a marked increase in local human population density. We next show that a nearby site with lower human impacts, El Garrapatero, currently manifests strong bimodality. This comparison suggests that bimodality can persist when human densities are low (Academy Bay in the past, El Garrapatero in the present), but not when they are high (Academy Bay in the present). Human activities may negatively impact diversification in 'young' adaptive radiations, perhaps by altering adaptive landscapes.     

Landscape moderation of biodiversity patterns and processes - eight hypotheses

Understanding how landscape characteristics affect biodiversity patterns and ecological processes at local and landscape scales is critical for mitigating effects of global environmental change. In this review, we use knowledge gained from human-modified landscapes to suggest eight hypotheses, which we hope will encourage more systematic research on the role of landscape composition and configuration in determining the structure of ecological communities, ecosystem functioning and services. We organize the eight hypotheses under four overarching themes. Section A: 'landscape moderation of biodiversity patterns' includes (1) the landscape species pool hypothesis-the size of the landscape-wide species pool moderates local (alpha) biodiversity, and (2) the dominance of beta diversity hypothesis-landscape-moderated dissimilarity of local communities determines landscape-wide biodiversity and overrides negative local effects of habitat fragmentation on biodiversity. Section B: 'landscape moderation of population dynamics' includes (3) the cross-habitat spillover hypothesis-landscape-moderated spillover of energy, resources and organisms across habitats, including between managed and natural ecosystems, influences landscape-wide community structure and associated processes and (4) the landscape-moderated concentration and dilution hypothesis-spatial and temporal changes in landscape composition can cause transient concentration or dilution of populations with functional consequences. Section C: 'landscape moderation of functional trait selection' includes (5) the landscape-moderated functional trait selection hypothesis-landscape moderation of species trait selection shapes the functional role and trajectory of community assembly, and (6) the landscape-moderated insurance hypothesis-landscape complexity provides spatial and temporal insurance, i.e. high resilience and stability of ecological processes in changing environments. Section D: 'landscape constraints on conservation management' includes (7) the intermediate landscape-complexity hypothesis-landscape-moderated effectiveness of local conservation management is highest in structurally simple, rather than in cleared (i.e. extremely simplified) or in complex landscapes, and (8) the landscape-moderated biodiversity versus ecosystem service management hypothesis-landscape-moderated biodiversity conservation to optimize functional diversity and related ecosystem services will not protect endangered species. Shifting our research focus from local to landscape-moderated effects on biodiversity will be critical to developing solutions for future biodiversity and ecosystem service management.     

When is sympatric speciation truly adaptive? An analysis of the joint evolution of resource utilization and assortative mating

The plausibility of sympatric speciation has long been debated among evolutionary ecologists. The process necessarily involves two key elements: the stable coexistence of at least two ecologically distinct types and the emergence of reproductive isolation. Recent theoretical studies within the theoretical framework of adaptive dynamics have shown how both these processes can be driven by natural selection. In the standard scenario, a population first evolves to an evolutionary branching point, next, disruptive selection promotes ecological diversification within the population, and, finally, the fitness disadvantage of intermediate types induces a selection pressure for assortative mating behaviour, which leads to reproductive isolation and full speciation. However, the full speciation process has been mostly studied through computer simulations and only analysed in part. Here I present a complete analysis of the whole speciation process by allowing for the simultaneous evolution of the branching ecological trait as well as a continuous trait controlling mating behaviour. I show how the joint evolution can be understood in terms of a gradient landscape, where the plausibility of different evolutionary paths can be evaluated graphically. I find sympatric speciation unlikely for scenarios with a continuous, unimodal, distribution of resources. Rather, ecological settings where the fitness inferiority of intermediate types is preserved during the ecological branching are more likely to provide opportunity for adaptive, sympatric speciation. Such scenarios include speciation due to predator avoidance or specialization on discrete resources. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Coevolution of slow-fast populations: evolutionary sliding, evolutionary pseudo-equilibria and complex Red Queen dynamics

We study the interplay of ecological and evolutionary dynamics in communities composed of populations with contrasting time-scales. In such communities, genetic variation of individual traits can cause population transitions between stationary and cyclic ecological regimes, hence abrupt variations in fitness. Such abrupt variations raise ridges in the adaptive landscape, where the populations are poised between equilibrium and cyclic coexistence and along which evolutionary trajectories can remain sliding for long times or halt at special points called evolutionary pseudo-equilibria. These novel phenomena should be generic to all systems in which ecological interactions cause fitness to vary discontinuously. They are demonstrated by the analysis of a predator-prey community, with one adaptive trait for each population. The eco-evolutionary dynamics of the system show a number of other distinctive features, including evolutionary extinction and two forms of Red Queen dynamics. One of them is characterized by intermittent bouts of cyclic oscillations of the two populations.     

Measuring the contribution of evolution to community trait structure in freshwater zooplankton

There are currently few predictions about when evolutionary processes are likely to play an important role in structuring community features. Determining predictors that indicate when evolution is expected to impact ecological processes in natural landscapes can help researchers identify eco-evolutionary ‘hotspots', where eco-evolutionary interactions are more likely to occur. Using data collected from a survey in freshwater cladoceran communities, landscape population genetic data and phenotypic trait data measured in a common garden, we applied a Bayesian linear model to assess whether the impact of local trait evolution in the keystone species Daphnia magna on cladoceran community trait values could be predicted by population genetic properties (within-population genetic diversity, genetic distance among populations), ecological properties (Simpson's diversity, phenotypic divergence) or environmental divergence. We found that the impact of local trait evolution varied among communities. Moreover, community diversity and phenotypic divergence were found to be better predictors of the contribution of evolution to community trait values than environmental features or genetic properties of the evolving species. Our results thus indicate the importance of ecological context for the impact of evolution on community features. Our study also demonstrates one way to detect signatures of eco-evolutionary interactions in communities inhabiting heterogeneous landscapes using survey data of contemporary ecological and evolutionary structure.     

Limiting similarity and functional diversity along environmental gradients

Recent developments in community models emphasize the importance of incorporating stochastic processes (e.g. ecological drift) in models of niche‐structured community assembly. We constructed a finite, spatially explicit, lottery model to simulate the distribution of species in a one‐dimensional landscape with an underlying gradient in environmental conditions. Our framework combines the potential for ecological drift with environmentally‐mediated competition for space in a heterogeneous environment. We examined the influence of niche breadth, dispersal distances, community size (total number of individuals) and the breadth of the environmental gradient on levels of species and functional trait diversity (i.e. differences in niche optima). Three novel results emerge from this model: (1) niche differences between adjacent species (e.g. limiting similarity) increase in smaller communities, because of the interaction of competitive effects and finite population sizes; (2) immigration from a regional species pool, stochasticity and niche‐assembly generate a bimodal distribution of species residence times (‘transient’ and ‘resident’) under a heterogeneous environment; and (3) the magnitude of environmental heterogeneity has a U‐shaped effect on diversity, because of shifts in species richness of resident vs. transient species. These predictions illustrate the potential importance of stochastic (although not necessarily neutral) processes in community assembly.     

A conceptual framework for the spatial analysis of functional trait diversity

Functional trait diversity is a popular tool in modern ecology, mainly used to infer assembly processes and ecosystem functioning. Patterns of functional trait diversity are shaped by ecological processes such as environmental filtering, species interactions and dispersal that are inherently spatial, and different processes may operate at different spatial scales. Adding a spatial dimension to the analysis of functional trait diversity may thus increase our ability to infer community assembly processes and to predict change in assembly processes following disturbance or land‐use change. Richness, evenness and divergence of functional traits are commonly used indices of functional trait diversity that are known to respond differently to large‐scale filters related to environmental heterogeneity and dispersal and fine‐scale filters related to species interactions (competition). Recent developments in spatial statistics make it possible to separately quantify large‐scale patterns (variation in local means) and fine‐scale patterns (variation around local means) by decomposing overall spatial autocorrelation quantified by Moran's coefficient into its positive and negative components using Moran eigenvector maps (MEM). We thus propose to identify the spatial signature of multiple ecological processes that are potentially acting at different spatial scales by contrasting positive and negative components of spatial autocorrelation for each of the three indices of functional trait diversity. We illustrate this approach with a case study from riparian plant communities, where we test the effects of disturbance on spatial patterns of functional trait diversity. The fine‐scale pattern of all three indices was increased in the disturbed versus control habitat, suggesting an increase in local scale competition and an overall increase in unexplained variance in the post‐disturbance versus control community. Further research using simulation modeling should focus on establishing the proposed link between community assembly rules and spatial patterns of functional trait diversity to maximize our ability to infer multiple processes from spatial community structure.     

Evolutionary ecology of inducible morphological plasticity in predator–prey interaction: toward the practical links with population ecology

The outcome of species interactions is often strongly influenced by variation in the functional traits of the individuals participating. A rather large body of work demonstrates that inducible morphological plasticity in predators and prey can both influence and be influenced by species interaction strength, with important consequences for individual fitness. Much of the past research in this area has focused on the ecological and evolutionary significance of trait plasticity by studying single predator–prey pairs and testing the performance of individuals having induced and noninduced phenotypes. This research has thus been critical in improving our understanding of the adaptive value of trait plasticity and its widespread occurrence across species and community types. More recently, researchers have expanded this foundation by examining how the complexity of organismal design and community-level properties can shape plasticity in functional traits. In addition, researchers have begun to merge evolutionary and ecological perspectives by linking trait plasticity to community dynamics, with particular attention on trait-mediated indirect interactions. Here, we review recent studies on inducible morphological plasticity in predators and their prey with an emphasis on internal and external constraints and how the nature of predator–prey interactions influences the expression of inducible phenotypes. In particular, we focus on multiple-trait plasticity, flexibility and modification of inducible plasticity, and reciprocal plasticity between predator and prey. Based on our arguments on these issues, we propose future research directions that should better integrate evolutionary and population studies and thus improve our understanding of the role of phenotypic plasticity in predator–prey population and community dynamics.     

Fitness and physiology in a variable environment

The relationship between physiological traits and fitness often depends on environmental conditions. In variable environments, different species may be favored through time, which can influence both the nature of trait evolution and the ecological dynamics underlying community composition. To determine how fluctuating environmental conditions favor species with different physiological traits over time, we combined long-term data on survival and fecundity of species in a desert annual plant community with data on weather and physiological traits. For each year, we regressed the standardized annual fitness of each species on its position along a tradeoff between relative growth rate and water-use efficiency. Next, we determined how variations in the slopes and intercepts of these fitness-physiology functions related to year-to-year variations in temperature and precipitation. Years with a relatively high percentage of small rain events and a greater number of days between precipitation pulse events tended to be worse, on average, for all desert annual species. Species with high relative growth rates and low water-use efficiency had greater standardized annual fitness than other species in years with greater numbers of large rain events. Conversely, species with high water-use efficiency had greater standardized annual fitness in years with small rain events and warm temperatures late in the growing season. These results reveal how weather variables interact with physiological traits of co-occurring species to determine interannual variations in survival and fecundity, which has important implications for understanding population and community dynamics.     

Coexistence through spatio-temporal heterogeneity and species sorting in grassland plant communities

The effect of spatial heterogeneity on species coexistence relies on the degree of niche heterogeneity in the habitat and the ability of species to exploit the available niche opportunities. We studied species coexistence in a perennial grassland, and tested whether small-scale disturbances create environmental heterogeneity that affects coexistence and whether the functional diversity of species in the species pool affects the ability of community composition to reflect heterogeneity through species sorting. We manipulated the spatio-temporal heterogeneity of disturbance and the functional diversity of species added as seed and measured their impact on the spatial turnover of species composition. Disturbance increased environmental heterogeneity and spatial turnover, and the effect of heterogeneity on turnover was greatest in the presence of a functionally diverse species pool, showing the importance of trait variation among species for exploiting environmental heterogeneity, and suggesting that coexistence occurred due to species sorting among heterogeneous niches.     

Adaptive landscape and functional diversity of Neotropical cichlids: implications for the ecology and evolution of Cichlinae (Cichlidae; Cichliformes)

Morphological, lineage and ecological diversity can vary substantially even among closely related lineages. Factors that influence morphological diversification, especially in functionally relevant traits, can help to explain the modern distribution of disparity across phylogenies and communities. Multivariate axes of feeding functional morphology from 75 species of Neotropical cichlid and a stepwise‐AIC algorithm were used to estimate the adaptive landscape of functional morphospace in Cichlinae. Adaptive landscape complexity and convergence, as well as the functional diversity of Cichlinae, were compared with expectations under null evolutionary models. Neotropical cichlid feeding function varied primarily between traits associated with ram feeding vs. suction feeding/biting and secondarily with oral jaw muscle size and pharyngeal crushing capacity. The number of changes in selective regimes and the amount of convergence between lineages was higher than expected under a null model of evolution, but convergence was not higher than expected under a similarly complex adaptive landscape. Functional disparity was compatible with an adaptive landscape model, whereas the distribution of evolutionary change through morphospace corresponded with a process of evolution towards a single adaptive peak. The continentally distributed Neotropical cichlids have evolved relatively rapidly towards a number of adaptive peaks in functional trait space. Selection in Cichlinae functional morphospace is more complex than expected under null evolutionary models. The complexity of selective constraints in feeding morphology has likely been a significant contributor to the diversity of feeding ecology in this clade.