Local adaptation at the range peripheries of Sitka spruce

High‐dispersal rates in heterogeneous environments and historical rapid range expansion can hamper local adaptation; however, we often see clinal variation in high‐dispersal tree species. To understand the mechanisms of the species’ distribution, we investigated local adaptation and adaptive plasticity in a range‐wide context in Sitka spruce, a wind‐pollinated tree species that has recently expanded its range after glaciations. Phenotypic traits were observed using growth chamber experiments that mimicked temperature and photoperiodic regimes from the limits of the species realized niche. Bud phenology exhibited parallel reaction norms among populations; however, putatively adaptive plasticity and strong divergent selection were seen in bud burst and bud set timing respectively. Natural selection appears to have favoured genotypes that maximize growth rate during available frost‐free periods in each environment. We conclude that Sitka spruce has developed local adaptation and adaptive plasticity throughout its range in response to current climatic conditions despite generally high pollen flow and recent range expansion.     

Habitat choice stabilizes metapopulation dynamics by enabling ecological specialization

Dispersal is a key trait responsible for the spread of individuals and genes among local populations, thereby generating eco‐evolutionary interactions. Especially in heterogeneous metapopulations, a tight coupling between dispersal, population dynamics and the evolution of local adaptation is expected. In this respect, dispersal should counteract ecological specialization by redistributing locally selected phenotypes (i.e. migration load). Habitat choice following an informed dispersal decision, however, can facilitate the evolution of ecological specialization. How such informed decisions influence metapopulation size and variability is yet to be determined. By means of individual‐based modelling, we demonstrate that informed decisions about both departure and settlement decouple the evolution of dispersal and that of generalism, selecting for highly dispersive specialists. Choice at settlement is based on information from the entire dispersal range, and therefore decouples dispersal from ecological specialization more effectively than choice at departure, which is only based on local information. Additionally, habitat choice at departure and settlement reduces local and metapopulation variability because of the maintenance of ecological specialization at all levels of dispersal propensity. Our study illustrates the important role of habitat choice for dynamics of spatially structured populations and thus emphasizes the importance of considering that dispersal is often informed.     

Climate‐mediated adaptation after mainland colonization of an ancestrally subtropical island lizard,Anolis carolinensis

Climate‐mediated evolution plays an integral role in species migration and range expansion. Gaining a clearer understanding of how climate affects demographic history and adaptation provides fundamental insight into the generation of intra‐ and interspecific diversity. In this study, we used the natural colonization of the green anole (Anolis carolinensis) from the island of Cuba to mainland North America to investigate the role of evolution at the niche, phenotypic and genetic levels after long‐term establishment in a novel environment. The North American green anole occupies a broader range of thermal habitats than its Cuban sister species. We documented niche expansion in the mainland green anole, mediated primarily through adaptation to winter temperatures. Common garden experiments strongly suggest a genetic component to differences in thermal performance found between populations in different temperature regimes. Analysis of geographic variation in population structure based on 53 486 single nucleotide variants from RAD loci revealed increased genetic isolation between populations in different vs. similar thermal environments. Selection scans for environment‐allele correlations reveal 19 genomic loci of known function that may have played a role in the physiological adaptation of A. carolinensis to temperate environments on the mainland.     

Canalization breakdown and evolution in a source-sink system

Understanding the process of adaptation to novel environments may help to elucidate several ecological phenomena, from the stability of species range margins to host-pathogen specificity and persistence in degraded habitats. We study evolution in one type of novel environment: a sink habitat where populations cannot persist without recurrent immigration from a source population. Previous studies on source-sink evolution have focused on how extrinsic environmental factors influence adaptation to a sink, but few studies have examined how intrinsic genetic factors influence adaptation. We use an individual-based model to explore how genetic canalization that evolves in gene regulation networks influences the adaptation of a population to a sink. We find that as canalization in the regulation network increases, the probability of adaptation to the novel habitat decreases. When adaptation to the habitat does occur, it is usually preceded by a breakdown of canalization. As evolution continues in the novel habitat, canalization reemerges, but a legacy of the breakdown may remain, even after several generations. We also find that environmental noise tends to increase the probability of adaptation to the novel habitat. Our results suggest that the details of genetic architecture can significantly influence the likelihood of niche evolution in novel environments.     

The learning advantage: bird species that learn their song show a tighter adjustment of song to noisy environments than those that do not learn

Song learning has evolved within several avian groups. Although its evolutionary advantage is not clear, it has been proposed that song learning may be advantageous in allowing birds to adapt their songs to the local acoustic environment. To test this hypothesis, we analysed patterns of song adjustment to noisy environments and explored their possible link to song learning. Bird vocalizations can be masked by low‐frequency noise, and birds respond to this by singing higher‐pitched songs. Most reports of this strategy involve oscines, a group of birds with learning‐based song variability, and it is doubtful whether species that lack song learning (e.g. suboscines) can adjust their songs to noisy environments. We address this question by comparing the degree of song adjustment to noise in a large sample of oscines (17 populations, 14 species) and suboscines (11 populations, 7 species), recorded in Brazil (Manaus, Brasilia and Curitiba) and Mexico City. We found a significantly stronger association between minimum song frequency and noise levels (effect size) in oscines than in suboscines, suggesting a tighter match in oscines between song transmission capacity and ambient acoustics. Suboscines may be more vulnerable to acoustic pollution than oscines and thus less capable of colonizing cities or acoustically novel habitats. Additionally, we found that species whose song frequency was more divergent between populations showed tighter noise–song frequency associations. Our results suggest that song learning and/or song plasticity allows adaptation to new habitats and that this selective advantage may be linked to the evolution of song learning and plasticity.     

Expansion history and environmental suitability shape effective population size in a plant invasion

The margins of an expanding range are predicted to be challenging environments for adaptation. Marginal populations should often experience low effective population sizes (N_e) where genetic drift is high due to demographic expansion and/or census population size is low due to unfavourable environmental conditions. Nevertheless, invasive species demonstrate increasing evidence of rapid evolution and potential adaptation to novel environments encountered during colonization, calling into question whether significant reductions in N_e are realized during range expansions in nature. Here we report one of the first empirical tests of the joint effects of expansion dynamics and environment on effective population size variation during invasive range expansion. We estimate contemporary values of N_e using rates of linkage disequilibrium among genome‐wide markers within introduced populations of the highly invasive plant Centaurea solstitialis (yellow starthistle) in North America (California, USA), and within native Eurasian populations. As predicted, we find that N_e within the invaded range is positively correlated with both expansion history (time since founding) and habitat quality (abiotic climate). History and climate had independent additive effects with similar effect sizes, indicating an important role for both factors in this invasion. These results support theoretical expectations for the population genetics of range expansion, though whether these processes can ultimately arrest the spread of an invasive species remains an unanswered question.     

Standing variation boosted by multiple sources of introduction contributes to the success of the introduced species, Lotus corniculatus

Although ecological differences between native and introduced ranges have been considered to drive rapid expansion of invasive species, recent studies suggest that rapid evolutionary responses of invasive species to local environments may also be common. Such expansion across heterogeneous environments by adaptation to local habitats requires genetic variation. In this study, we investigated the source and role of standing variation in successful invasion of heterogeneous abiotic environments in a self-incompatible species, Lotus corniculatus. We compared phenotypic and genetic variation among cultivars, natives, and introduced genotypes, and found substantial genetic variation within both native and introduced populations. Introduced populations possessed genotypes derived from both cultivars and native populations, and had lower population differentiation, indicating multiple sources of introduction and population admixture among the sources in the introduced range. Both cultivars and introduced populations had similarly outperforming phenotypes on average, with increased biomass and earlier flowering compared with native populations, but those phenotypes were within the range of the variation in phenotypes of the native populations. In addition, clinal variation within introduced populations was detected along a climatic gradient. Multiple introductions from different sources, including cultivars, may have contributed to pre-adaptive standing variation in the current introduced populations. We conclude that both introduction of cultivar genotypes and natural selection in local environments contributed to current patterns of genetic and phenotypic variation observed in the introduced populations.     

Historical demographic dynamics underlying local adaptation in the presence of gene flow

The range of a species is the result of the relative contribution of spatial tracking of environmental requirements and adaptation to ecological conditions outside the ancestral niche. The appearance of novel habitats caused by climatic oscillation can promote range expansion and accompanying demographic growth. The demographic dynamics of populations leave a signal in \ patterns. We modeled three competing scenarios pertaining to the circumstance of a range expansion by the Karoo Scrub‐Robin into newly available habitat resulting from the increasing aridification of southern Africa. Genetic variation was contrasted with the theoretical expectations of a spatial range expansion, and compared with data of a putative adaptive trait. We infer that this bird likely colonized the arid zone, as a consequence of adaptive evolution in a small peripheral population, followed by an expansion with recurrent exchange of migrants with the ancestral populations.     

Mating timing,dispersal and local adaptation in patchy environments

Dispersal is a life‐history trait that can evolve under various known selective pressures as identified by a multitude of theoretical and empirical studies. Yet only few of them are considering the succession of mating and dispersal. The sequence of these events influences gene flow and consequently affects the dynamics and evolution of populations. We use individual‐based simulations to investigate the evolution of the timing of dispersal and mating, i.e. mating before or after dispersal. We assume a discrete insect metapopulation in a heterogeneous environment, where populations may adapt to local conditions and only females are allowed to disperse. We run the model assuming different levels of species habitat tolerance, carrying capacity, and temporal environmental variability. Our results show that in species with narrow habitat tolerance, low to moderate dispersal evolves in combination with mating after dispersal (post‐dispersal mating). With such a strategy dispersing females benefit from mating with a resident male, as their offspring will be better adapted to the local habitat conditions. On the contrary, in species with wide habitat tolerance higher dispersal rates in combination with pre‐dispersal mating evolves. In this case individuals are adapted to the ‘average’ habitat where pre‐dispersal mating conveys the benefit of carrying relatives’ genes into a new population. With high dispersal rates and large population size, local adaptation and kin structure both vanish and the temporal sequence of dispersal and mating may become a (nearly) neutral trait.     

Fitness declines towards range limits and local adaptation to climate affect dispersal evolution during climate‐induced range shifts

Dispersal ability will largely determine whether species track their climatic niches during climate change, a process especially important for populations at contracting (low‐latitude/low‐elevation) range limits that otherwise risk extinction. We investigate whether dispersal evolution at contracting range limits is facilitated by two processes that potentially enable edge populations to experience and adjust to the effects of climate deterioration before they cause extinction: (i) climate‐induced fitness declines towards range limits and (ii) local adaptation to a shifting climate gradient. We simulate a species distributed continuously along a temperature gradient using a spatially explicit, individual‐based model. We compare range‐wide dispersal evolution during climate stability vs. directional climate change, with uniform fitness vs. fitness that declines towards range limits (RLs), and for a single climate genotype vs. multiple genotypes locally adapted to temperature. During climate stability, dispersal decreased towards RLs when fitness was uniform, but increased when fitness declined towards RLs, due to highly dispersive genotypes maintaining sink populations at RLs, increased kin selection in smaller populations, and an emergent fitness asymmetry that favoured dispersal in low‐quality habitat. However, this initial dispersal advantage at low‐fitness RLs did not facilitate climate tracking, as it was outweighed by an increased probability of extinction. Locally adapted genotypes benefited from staying close to their climate optima; this selected against dispersal under stable climates but for increased dispersal throughout shifting ranges, compared to cases without local adaptation. Dispersal increased at expanding RLs in most scenarios, but only increased at the range centre and contracting RLs given local adaptation to climate.     

Niche conservatism among non‐native vertebrates in Europe and North America

Niche conservatism, the hypothesis that niches remain constant through time and space, is crucial for the study of biological invasions as it underlies native‐range based predictions of invasion risk. Niche changes between native and non‐native populations are increasingly reported. However, it has been argued that these changes arise mainly because in their novel range, species occupy only a subset of the environments they inhabit in their native range, and not because they expand into environments entirely novel to them. Here, using occurrences of 29 vertebrate species native to either Europe or North America and introduced into the other continent, we assess the prevalence of niche changes between native and non‐native populations and assess whether the changes detected are caused primarily by native niche unfilling in the non‐native range rather than by expansion into novel environments. We show that niche overlap between native and non‐native populations is generally low because of a large degree of niche unfilling in the non‐native range. This most probably reflects an ongoing colonization of the novel range, as niche changes were smaller for species that were introduced longer ago and into a larger number of locations. Niche expansion was rare, and for the few species exhibiting larger amounts of niche overlap, an unfilling of the niche in the native range (e.g. through competition or dispersal limitations) is the most probable explanation. The fact that for most species, the realized non‐native niche is a subset of the realized native niche allows native‐range based niche models to generate accurate predictions of invasion risk. These results suggest that niche changes arising during biological invasions are strongly influenced by propagule pressure and colonization processes, and we argue that introduction history should be taken into account when evaluating niche conservatism in the context of biological invasions.     

The genetics of adaptation to discrete heterogeneous environments: frequent mutation or large‐effect alleles can allow range expansion

Range expansions are complex evolutionary and ecological processes. From an evolutionary standpoint, a populations' adaptive capacity can determine the success or failure of expansion. Using individual‐based simulations, we model range expansion over a two‐dimensional, approximately continuous landscape. We investigate the ability of populations to adapt across patchy environmental gradients and examine how the effect sizes of mutations influence the ability to adapt to novel environments during range expansion. We find that genetic architecture and landscape patchiness both have the ability to change the outcome of adaptation and expansion over the landscape. Adaptation to new environments succeeds via many mutations of small effect or few of large effect, but not via the intermediate between these cases. Higher genetic variance contributes to increased ability to adapt, but an alternative route of successful adaptation can proceed from low genetic variance scenarios with alleles of sufficiently large effect. Steeper environmental gradients can prevent adaptation and range expansion on both linear and patchy landscapes. When the landscape is partitioned into local patches with sharp changes in phenotypic optimum, the local magnitude of change between subsequent patches in the environment determines the success of adaptation to new patches during expansion.     

Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis)

The traditional view of the species as the fundamental unit of evolution has been challenged by observations that in heterogeneous environments, gene flow may be too restricted to overcome the effects of local selection. Whether a species evolves as a cohesive unit depends critically on the dynamic balance between homogenizing gene flow among populations and potentially disruptive local adaptation. To examine this evolutionary balance between "global" gene flow and local selection, we studied northern Californian populations of Helianthus exilis, the serpentine sunflower, within a mosaic of contrasting serpentine and nonserpentine areas that differ considerably in soil chemistry and water availability. Local adaptation to riparian and serpentine habitats was studied in Helianthus exilis along with an analysis of gene flow patterns among populations within these habitats. Local adaptation was assessed in H. exilis during 2002 and 2003 using reciprocal transplant experiments at multiple locations within serpentine and riparian habitats. Effects of competition and germination date on the expression of local adaptation were also examined within the reciprocal transplant experiments. Local adaptation was detected in both years at the local site level and at the level of habitat. The analysis of the transplanted populations indicated that the patterns of selection differed considerably between riparian and serpentine sites. Differential survivorship occurred in serpentine habitats, whereas selection on reproductive output predominated in riparian habitats. Local adaptation was expressed only in the absence of competition. Local adaptation in terms of survivorship was most strongly expressed in treatments with delayed seed germination. Microsatellite markers were used to quantify population genetic parameters and examine the patterns of gene flow among sampled populations. Analysis of molecular markers revealed a system of population patches that freely exchange genes with each other. Strong selection seems to maintain ecotypic variation within this endemic sunflower species, while extensive gene flow among populations prevents local speciation between serpentine and riparian ecotypes.     

LOCAL ADAPTATION IN A CHANGING WORLD: THE ROLES OF GENE‐FLOW,MUTATION, AND SEXUAL REPRODUCTION

In spatially heterogeneous environments, the processes of gene flow, mutation, and sexual reproduction generate local genetic variation and thus provide material for local adaptation. On the other hand, these processes interchange maladapted for adapted genes and so, in each case, the net influence may be to reduce local adaptation. Previous work has indicated that this is the case in stable populations, yet it is less clear how the factors play out during population growth, and in the face of temporal environmental stochasticity. We address this issue with a spatially explicit, stochastic model. We find that dispersal, mutation, and sexual reproduction can all accelerate local adaptation in growing populations, although their respective roles may depend on the genetic make‐up of the founding population. All three processes reduce local adaptation, however, in the long term, that is when population growth becomes balanced by density‐dependent competition. These relationships are qualitatively maintained, although quantitatively reduced, if the resources are locally ephemeral. Our results suggest that species with high levels of local adaptation within their ranges may not be the same species that harbor potential for rapid local adaptation during population expansion.     

The experimental evolution of specialists,generalists, and the maintenance of diversity

Environmental heterogeneity may be a general explanation for both the quantity of genetic variation in populations and the ecological niche width of individuals. To evaluate this hypothesis, I review the literature on selection experiments in heterogeneous environments. The niche width usually – but not invariably – evolves to match the amount of environmental variation, specialists evolving in homogeneous environments and generalists evolving in heterogeneous environments. The genetics of niche width are more complex than has previously been recognized, particularly with respect to the magnitude of costs of adaptation and the putative constraints on the evolution of generalists. Genetic variation in fitness is more readily maintained in heterogeneous environments than in homogeneous environments and this diversity is often stably maintained through negative frequency‐dependent selection. Moreover environmental heterogeneity appears to be a plausible mechanism for at least two well‐known patterns of species diversity at the landscape scale. I conclude that environmental heterogeneity is a plausible and possibly very general explanation for diversity across the range of scales from individuals to landscapes.     

Predicting range shifts under global change: the balance between local adaptation and dispersal

Bioclimate envelope models (BEMs) have often been criticized as being too simplistic due to e.g. not incorporating effects of biotic interactions or evolutionary adaptation. However, BEMs are widely applied and have proven to be often useful. Here we investigate, under which conditions evolution of dispersal, local adaptation or interspecific competition may be of minor importance for forecasting future range shifts. Therefore we use individual‐based simulations of metapopulations under climate change living in spatial temperature gradients. Scenarios incorporate single‐species systems or systems with competing species, respectively. Dispersal rate is evolving and adaptation to local conditions may also evolve in some scenarios. Results show that in single‐species scenarios excluding evolutionary adaptation, species either follow optimal habitat conditions or go extinct if habitat connectivity is too low. These simulations are in close accordance to predictions from BEMs. Including evolutionary adaptation qualitatively changes these results. In the absence of competing species the species either completely invades the world or goes extinct. With competitors, results strongly depend on habitat fragmentation. For highly connected habitats the range border may shift as predicted by BEMs, for intermediate connectivity it will lag behind, while species will go extinct if fragmentation is too high. Our results indicate that (simple) BEMs may work well if habitats are well connected and species will not encounter many difficulties in dispersing to new sites. Selection in this case may promote evolution of even higher dispersal activities. We thus show that the presence of biotic interactions may be ignored for predictions of range shifts when high dispersal can be expected.     

Evolutionary genomics of gypsy moth populations sampled along a latitudinal gradient

The European gypsy moth (Lymantria dispar L.) was first introduced to Massachusetts in 1869 and within 150 years has spread throughout eastern North America. This large‐scale invasion across a heterogeneous landscape allows examination of the genetic signatures of adaptation potentially associated with rapid geographical spread. We tested the hypothesis that spatially divergent natural selection has driven observed changes in three developmental traits that were measured in a common garden for 165 adult moths sampled from six populations across a latitudinal gradient covering the entirety of the range. We generated genotype data for 91,468 single nucleotide polymorphisms based on double digest restriction‐site associated DNA sequencing and used these data to discover genome‐wide associations for each trait, as well as to test for signatures of selection on the discovered architectures. Genetic structure across the introduced range of gypsy moth was low in magnitude (F_ST = 0.069), with signatures of bottlenecks and spatial expansion apparent in the rare portion of the allele frequency spectrum. Results from applications of Bayesian sparse linear mixed models were consistent with the presumed polygenic architectures of each trait. Further analyses indicated spatially divergent natural selection acting on larval development time and pupal mass, with the linkage disequilibrium component of this test acting as the main driver of observed patterns. The populations most important for these signals were two range‐edge populations established less than 30 generations ago. We discuss the importance of rapid polygenic adaptation to the ability of non‐native species to invade novel environments.     

High‐throughput sequencing of transposable element insertions suggests adaptive evolution of the invasive Asian tiger mosquito towards temperate environments

Invasive species represent unique opportunities to evaluate the role of local adaptation during colonization of new environments. Among these species, the Asian tiger mosquito, Aedes albopictus, is a threatening vector of several human viral diseases, including dengue and chikungunya, and raises concerns about the Zika fever. Its broad presence in both temperate and tropical environments has been considered the reflection of great “ecological plasticity.” However, no study has been conducted to assess the role of adaptive evolution in the ecological success of Ae. albopictus at the molecular level. In the present study, we performed a genomic scan to search for potential signatures of selection leading to local adaptation in one‐hundred‐forty field‐collected mosquitoes from native populations of Vietnam and temperate invasive populations of Europe. High‐throughput genotyping of transposable element insertions led to the discovery of more than 120,000 polymorphic loci, which, in their great majority, revealed a virtual absence of structure between the biogeographic areas. Nevertheless, 92 outlier loci showed a high level of differentiation between temperate and tropical populations. The majority of these loci segregate at high insertion frequencies among European populations, indicating that this pattern could have been caused by recent adaptive evolution events in temperate areas. An analysis of the overlapping and neighbouring genes highlighted several candidates, including diapause, lipid and juvenile hormone pathways.     

ECOLOGICAL HISTORY AND EVOLUTION IN A NOVEL ENVIRONMENT: HABITAT HETEROGENEITY AND INSECT ADAPTATION TO A NEW HOST PLANT

Environmental heterogeneity has often been implicated in the maintenance of genetic variation. However, previous research has not considered how environmental heterogeneity might affect the rate of adaptation to a novel environment. In this study, I used an insect-plant system to test the hypothesis that heterogeneous environments maintain more genetic variation in fitness components in a novel environment than do uniform environments. To manipulate recent ecological history, replicate populations of the dipteran leafminer Liriomyza trifolii were maintained for 20 generations in one of three treatments: a heterogeneous environment that contained five species of host plant, and two uniform environments that contained either a susceptible chrysanthemum or tomato. The hypothesis that greater genetic variance for survivorship and developmental time on a new host plant (a leafminer-resistant chrysanthemum) would be maintained in the heterogeneous treatment relative to the uniform environments was then tested with a sib-analysis and a natural selection experiment. Populations from the heterogeneous host plant treatment had no greater genetic variance in either larval survivorship or developmental time on the new host than did populations from either of the other treatments. Moreover, the rate of adaptation to the new host did not differ between the ecological history treatments, although the populations from the uniform chrysanthemum treatment had higher mean survivorship throughout the selection experiment. The estimates of the heritability of larval survivorship from the sib-analysis and selection experiment were quite similar. These results imply that ecologically realistic levels of environmental heterogeneity will not necessarily maintain more genetic variance than uniform environments when traits expressed in a particular novel environment are considered.     

Conceptual issues in local adaptation

Studies of local adaptation provide important insights into the power of natural selection relative to gene flow and other evolutionary forces. They are a paradigm for testing evolutionary hypotheses about traits favoured by particular environmental factors. This paper is an attempt to summarize the conceptual framework for local adaptation studies. We first review theoretical work relevant for local adaptation. Then we discuss reciprocal transplant and common garden experiments designed to detect local adaptation in the pattern of deme × habitat interaction for fitness. Finally, we review research questions and approaches to studying the processes of local adaptation – divergent natural selection, dispersal and gene flow, and other processes affecting adaptive differentiation of local demes. We advocate multifaceted approaches to the study of local adaptation, and stress the need for experiments explicitly addressing hypotheses about the role of particular ecological and genetic factors that promote or hinder local adaptation. Experimental evolution of replicated populations in controlled spatially heterogeneous environments allow direct tests of such hypotheses, and thus would be a valuable way to complement research on natural populations.