Interspecific Competition, Environmental Gradients, Gene Flow, and the Coevolution of Species' Borders

Darwin viewed species range limits as chiefly determined by an interplay between the abiotic environment and interspecific interactions. Haldane argued that species' ranges could be set intraspecifically when gene flow from a species' populous center overwhelms local adaptation at the periphery. Recently, Kirkpatrick and Barton have modeled Haldane's process with a quantitative genetic model that combines density-dependent local population growth with dispersal and gene flow across a linear environmental gradient in optimum phenotype. To address Darwin's ideas, we have extended the Kirkpatrick and Barton model to include interspecific competition and the frequency-dependent selection that it generates, as well as stabilizing selection on a quantitative character. Our model includes local population growth, movements over space, natural selection, and gene flow. It simultaneously addresses the evolution of character displacement and species borders. It reproduces the Kirkpatrick and Barton single-species result that limited ranges can be produced with sufficiently steep environmental gradients and strong dispersal. Further, in the absence of environmental gradients or barriers to dispersal, interspecific competition will not limit species ranges at evolutionary equilibrium. However, interspecific competition can interact with environmental gradients and gene flow to generate limited ranges with much less extreme gradient and dispersal parameters than in the single-species case. Species display character displacement in sympatry, yet the reduction in competition that results from this displacement does not necessarily allow the two species to become sympatric everywhere. When species meet, competition reduces population densities in the region of overlap, which, in turn, intensifies the asymmetry in gene flow from center to margin. This reduces the ability of each species to adapt to local physical conditions at their range limits. If environmental gradients are monotonic but not linear, the transition zone between species at coevolutionary equilibrium occurs where the environmental gradient is steepest. If productivity gradients are also introduced into the model, then patterns similar to Rapoport's rule emerge. Interacting species respond to climate change, as it affects the optimal phenotype over space, by a combination of range shifts and local evolution in mean phenotype, while solitary species respond solely by range shifts. Finally, we compare empirical estimates for intrinsic growth rates and diffusion coefficients for several species to those needed by the single-species model to produce a stable limited range. These empirical values are generally insufficient to produce limited ranges in the model suggesting a role for interspecific interactions.     

Genetic differentiation across a latitudinal gradient in two co-occurring butterfly species: revealing population differences in a context of climate change

Genetic differentiation within a species' range is determined by natural selection, genetic drift, and gene flow. Selection and drift enhance genetic differences if populations are sufficiently isolated, while gene flow precludes differentiation and local adaptation. Over large geographical areas, these processes can create a variety of scenarios, ranging from admixture to a high degree of population differentiation. Genetic differences among populations may signal functional differences within a species' range, potentially leading to population or ecotype-specific responses to global change. We investigated differentiation within the geographical range of two butterfly species along a broad latitudinal gradient. This gradient is the primary axis of climatic variation, and many ecologists expect populations at the poleward edge of this gradient to expand under climate change. Our study species inhabit a shared ecosystem and differ in body size and resource specialization; both also find their poleward range limit on an island. We find evidence for divergence of peripheral populations from the core in both taxa, suggesting the potential for genetic distinctiveness at the leading edge of climate change. We also find differences between the species in the extent of peripheral differentiation with the smaller and more specialized species showing greater population divergence (microsatellites and mtDNA) and reduced gene flow (mtDNA). Finally, gene flow estimates in both species differed strongly between two marker types. These findings suggest caution in assuming that populations are invariant across latitude and thus will respond as a single ecotype to climatic change.     

Predation and the evolutionary dynamics of species ranges

Gene flow that hampers local adaptation can constrain species distributions and slow invasions. Predation as an ecological factor mainly limits prey species ranges, but a richer array of possibilities arises once one accounts for how predation alters the interplay of gene flow and selection. We extend previous single-species theory on the interplay of demography, gene flow, and selection by investigating how predation modifies the coupled demographic-evolutionary dynamics of the range and habitat use of prey. We consider a model for two discrete patches and a complementary model for species along continuous environmental gradients. We show that predation can strongly influence the evolutionary stability of prey habitat specialization and range limits. Predators can permit prey to expand in habitat or geographical range or, conversely, cause range collapses. Transient increases in predation can induce shifts in prey ranges that persist even if the predator itself later becomes extinct. Whether a predator tightens or loosens evolutionary constraints on the invasion speed and ultimate size of a prey range depends on the predator effectiveness, its mobility relative to its prey, and the prey's intraspecific density dependence, as well as the magnitude of environmental heterogeneity. Our results potentially provide a novel explanation for lags and reversals in invasions.     

Species' borders and dispersal barriers

Range limits of species are determined by combined effects of physical, historical, ecological, and evolutionary forces. We consider a subset of these factors by using spatial models of competition, hybridization, and local adaptation to examine the effects of partial dispersal barriers on the locations of borders between similar species. Prompted by results from population genetic models and biogeographic observations, we investigate the conditions under which species' borders are attracted to regions of reduced dispersal. For borders maintained by competition or hybridization, we find that dispersal barriers can attract borders whose positions would otherwise be either neutrally stable or moving across space. Borders affected strongly by local adaptation and gene flow, however, are repelled from dispersal barriers. These models illustrate how particular biotic and abiotic factors may combine to limit species' ranges, and they help to elucidate mechanisms by which range limits of many species may coincide.     

Body mass explains characteristic scales of habitat selection in terrestrial mammals

Niche theory in its various forms is based on those environmental factors that permit species persistence, but less work has focused on defining the extent, or size, of a species' environment: the area that explains a species' presence at a point in space. We proposed that this habitat extent is identifiable from a characteristic scale of habitat selection, the spatial scale at which habitat best explains species' occurrence. We hypothesized that this scale is predicted by body size. We tested this hypothesis on 12 sympatric terrestrial mammal species in the Canadian Rocky Mountains. For each species, habitat models varied across the 20 spatial scales tested. For six species, we found a characteristic scale; this scale was explained by species' body mass in a quadratic relationship. Habitat measured at large scales best-predicted habitat selection in both large and small species, and small scales predict habitat extent in medium-sized species. The relationship between body size and habitat selection scale implies evolutionary adaptation to landscape heterogeneity as the driver of scale-dependent habitat selection.     

A multilocus population genetic survey of the greater sage-grouse across their range

The distribution and abundance of the greater sage-grouse (Centrocercus urophasianus) have declined dramatically, and as a result the species has become the focus of conservation efforts. We conducted a range-wide genetic survey of the species which included 46 populations and over 1000 individuals using both mitochondrial sequence data and data from seven nuclear microsatellites. Nested clade and structure analyses revealed that, in general, the greater sage-grouse populations follow an isolation-by-distance model of restricted gene flow. This suggests that movements of the greater sage-grouse are typically among neighbouring populations and not across the species, range. This may have important implications if management is considering translocations as they should involve neighbouring rather than distant populations to preserve any effects of local adaptation. We identified two populations in Washington with low levels of genetic variation that reflect severe habitat loss and dramatic population decline. Managers of these populations may consider augmentation from geographically close populations. One population (Lyon/Mono) on the southwestern edge of the species' range appears to have been isolated from all other greater sage-grouse populations. This population is sufficiently genetically distinct that it warrants protection and management as a separate unit. The genetic data presented here, in conjunction with large-scale demographic and habitat data, will provide an integrated approach to conservation efforts for the greater sage-grouse.     

The evolution of species interactions across natural landscapes

Given the potential for rapid and microgeographical adaptation, ecologists increasingly are exploring evolutionary explanations for community patterns. Biotic selection can generate local adaptations that alter species interactions. Although some gene flow might be necessary to fuel local adaptation, higher gene flow can homogenise traits across regions and generate local maladaptation. Herein, I estimate the contributions of local biotic selection, gene flow and spatially autocorrelated biotic selection to among-population divergence in traits involved in species interactions across 75 studies. Local biotic selection explained 6.9% of inter-population trait divergence, an indirect estimate of restricted gene flow explained 0.1%, and spatially autocorrelated selection explained 9.3%. Together, biotic selection explained 16% of the variance in population trait means. Most biotic selection regimes were spatially autocorrelated. Hence, most populations receive gene flow from populations facing similar selection, which could allow for local adaptation despite moderate gene flow. Gene flow constrained adaptation in studies conducted at finer spatial scales as expected, but this effect was often confounded with spatially autocorrelated selection. Results indicate that traits involved in species interactions might often evolve across landscapes, especially when biotic selection is spatially autocorrelated. The frequent evolution of species interactions suggests that evolutionary processes might often influence community ecology.     

Nonrandom larval dispersal can steepen marine clines

Sharp and stable clinal variation is enigmatic when found in species with high gene flow. Classical population genetic models treat gene flow as a random homogenizing force countering local adaptation across habitat discontinuities. Under this view, dispersal over large spatial scales will lower the effectiveness of adaptation by natural selection at finer spatial scales. Thus, random gene flow will create a shallow phenotypic cline across an ecotone in response to a steep selection gradient. In sedentary marine species that disperse primarily as larvae, nonrandom dispersal patterns are expected due to coastal hydrodynamics. Surprisingly sharp phenotypic and genotypic clines have been documented in marine species with high gene flow. We are interested in the extent to which nonrandom dispersal could accentuate such clines. We model a linear species range in which populations have stable and uniform densities along a selection gradient; in contrast to random dispersal, convergent advection of larvae can amplify phenotypic differentiation if coupled with a semipermeable dispersal barrier in the convergence zone. The migration load caused by directional dispersal pushes the phenotypic mean away from the local trait optimum in downstream populations, that is, near the convergence zone. A dispersal barrier is possible as a result of colliding currents if the water and larvae are mostly displaced offshore, away from suitable settlement habitat. Disjunctions in a quantitative trait were enlarged in the convergence zone by faster current flows or a more complete dispersal barrier. With advection of larvae per generation one-third as far as the average dispersal distance by diffusion, convergence on a dispersal barrier with 40% permeability generated a trait disjunction across the convergence zone of two phenotypic standard deviations. Without directional dispersal, similar clines also developed across a habitat gap, where population density was low, or across dispersal barriers with less than 1% permeability. These findings suggest that the types of hydrographic phenomena often associated with marine transition zones can strongly affect the balance between gene flow and selection and generate surprisingly steep clines given the large-scale gene flow expected from larvae.     

Genetic diversity and gene flow in a rare New Zealand skink despite fragmented habitat in a volcanic landscape

Anthropogenic habitat fragmentation often restricts gene flow and results in small populations that are at risk of inbreeding. However, some endangered species naturally occupy patchy habitat where local population extinction and recolonization are normal. We investigated population fragmentation in the range‐restricted New Zealand small‐scaled skink (Oligosoma microlepis), documenting changes in habitat occupancy and analyzing mitochondrial, microsatellite, and morphological variation sampled across the geographical range of the species (approximately 100 km²). Small‐scaled skinks have a strong preference for rocky outcrops that exist in a mosaic of other habitat types. A metapopulation structure was indicated by both local extinction and colonization of new sites. We found relatively high mtDNA nucleotide site diversity within this narrow range (π = 0.004; 16S), evidence of inter‐patch gene flow, and no statistical support for inbreeding. Gene flow was limited by geographical distance, although the existence of pasture between habitat patches apparently has not prevented skink dispersal. Generalized linear models indicated an association between body size and location suggesting a local environmental influence on phenotype. Prior to human‐induced habitat modification, native forest probably separated preferred sites and, less than 2000 years ago, volcanic activity devastated much of the area currently occupied by O. microlepis. This skink appears able to re‐establish populations if other human‐linked factors such as agricultural intensification and introduced predators are limited. Although in contrast to expectations for a scarce and localized species living in a highly modified landscape, this lizard may have previously adapted to a dynamic, mosaic environment mediated by volcanism.     

Species range expansion by beneficial mutations

A species' range can be limited when there is no genetic variation for a trait that allows for adaptation to more extreme environments. We study how range expansion occurs by the establishment of a new mutation that affects a quantitative trait in a spatially continuous population. The optimal phenotype for the trait varies linearly in space. The survival probabilities of new mutations affecting the trait are found by simulation. Shallow environmental gradients favour mutations that arise nearer to the range margin and that have smaller phenotypic effects than do steep gradients. Mutations that become established in shallow environmental gradients typically result in proportionally larger range expansions than those that establish in steep gradients. Mutations that become established in populations with high maximum growth rates tend to originate nearer to the range edge and to cause relatively smaller range expansion than mutations that establish in populations with low maximum growth rates. Under plausible parameter values, mutations that allow for range expansion tend to have large phenotypic effects (more than one phenotypic standard deviation) and cause substantial range expansions (15% or more). Sexual reproduction allows for larger range expansions and adaptation to more extreme environments than asexual reproduction.     

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.     

Responses of 'resistant' vertebrates to habitat loss and fragmentation: the importance of niche breadth and range boundaries

Abstract. An ability to predict species' sensitivities to habitat loss and fragmentation has important conservation implications, and numerous hypotheses have been proposed to explain interspecific differences observed in human-dominated landscapes. We used occupancy data collected on 32 species of vertebrates (16 mammals and 16 amphibians) in an agricultural landscape of Indiana, USA, to compare hypotheses that focus on different causal mechanisms underlying interspecific variation in responses to habitat alteration: (1) body size; (2) morphology and development; (3) behaviour; (4) niche breadth; (5) proximity to range boundary; and multiple-process models combining main effects and interactions of hypotheses (1)–(2) and (4)–(5). The majority of habitat alteration occurred over a century ago and coincided with extinction of several species; thus, our study dealt only with variation in responses of extant species that often are considered 'resistant' to human modifications of native habitat. Corrected Akaike scores and Akaike weights provided strongest support for models incorporating niche breadth and proximity to range boundary. Measures of dietary and habitat breadth obtained from the literature were negatively correlated with sensitivity to habitat alteration. Additionally, greater sensitivity was observed for species occurring at the periphery of their geographical ranges, especially at northern or western margins. Body size, morphological, developmental and behavioural traits were inferior predictors of tolerance to fragmentation for the species and landscape we examined. Our findings reinforce the importance of niche breadth as a predictor of species' responses to habitat alteration. They also highlight the importance of viewing the effects of habitat loss and fragmentation in a landscape within a biogeographical context that considers a species' level of adaptation to local environmental conditions.     

Population dynamics and evolutionary processes: the manifold roles of habitat selection

Summary Any character that has a substantial effect on a species' distribution and abundance can exert a variety of indirect effects on evolutionary processes. It is suggested that an organism's capacity for habitat selection is just such a character. Habitat selection can constrain the selective environment experienced by a population. Habitat selection can also indirectly influence the relative importance of natural selection, drift, and gene flow, through its effect on population size and growth rate. In many circumstances (but not all), habitat selection increases population size and growth rate, and thereby makes selection in a local environment more effective than drift and gene flow.     

Allee effects, invasion pinning, and species' borders

All species' ranges are the result of successful past invasions. Thus, models of species' invasions and their failure can provide insight into the formation of a species' geographic range. Here, we study the properties of invasion models when a species cannot persist below a critical population density known as an "Allee threshold." In both spatially continuous reaction-diffusion models and spatially discrete coupled ordinary-differential-equation models, the Allee effect can cause an invasion to fail. In patchy landscapes (with dynamics described by the spatially discrete model), range limits caused by propagation failure (pinning) are stable over a wide range of parameters, whereas, in an uninterrupted habitat (with dynamics described by a spatially continuous model), the zero velocity solution is structurally unstable and thus unlikely to persist in nature. We derive conditions under which invasion waves are pinned in the discrete space model and discuss their implications for spatially complex dynamics, including critical phenomena, in ecological landscapes. Our results suggest caution when interpreting abrupt range limits as stemming either from competition between species or a hard environmental limit that cannot be crossed: under a wide range of plausible ecological conditions, species' ranges may be limited by an Allee effect. Several example systems appear to fit our general model.     

Matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology

Gene flow among populations is typically thought to be antagonistic to population differentiation and local adaptation. However, this assumes that dispersing individuals disperse randomly with respect to their ability to use the environment. Yet dispersing individuals often sample and compare environments and settle in those environments that best match their phenotype, causing directed gene flow, which can in fact promote population differentiation and adaptation. We refer to this process as "matching habitat choice." Although this process has been acknowledged by several researchers, no synthesis or perspective on its potentially widespread importance exists. Here we synthesize empirical and theoretical studies, and offer a new perspective that matching habitat choice can have significant effects on important and controversial topics. We discuss the potential implications of matching habitat choice for the degree and rate of local adaptation, the evolution of niche width, adaptive peak shifts, speciation in the presence of gene flow, and on our view and interpretation of measures of natural selection. Because of its potential importance for such a wide range of topics, we call for heightened empirical and theoretical attention for this neglected dimension in evolutionary and ecological studies.     

Time as an ecological constraint

Conventional approaches to population biology emphasise the roles of climatic conditions, nutrient flow and predation as constraints on population dynamics. We argue here that this focus has obscured the role of time as a crucial constraint on species' abilities to survive in some habitats. Time constraints may be particularly intrusive both for species that live in intensely bonded groups (where the need to devote time to social interaction may ultimately limit the size of group that a species can maintain in a particular habitat) and for taxa that face constraints on the length of the active day. We use a linear programming approach that allows us to specify both how time allocations to different activities are influenced by local environmental and climatic variables and how these in turn limit group size and population density. The linear programming approach identifies the realizable niche space within which a species can maintain coherent groups that are larger than the minimum viable group size (or density). This approach thus allow us to understand better why a given taxon can survive in some habitats but not others, as well as the demographic stress that a population may face. In addition, they also allow us to evaluate the implications of both past and future climate change for a taxon's ability to cope with particular habitats.     

Quantifying the impact of gene flow on phenotype-environment mismatch: a demonstration with the scarlet monkeyflower Mimulus cardinalis

Geographic range margins offer testing grounds for limits to adaptation. If range limits are concordant with niche limits, range expansions require the evolution of new phenotypes that can maintain populations beyond current range margins. However, many species' range margins appear static over time, suggesting limits on the ability of marginal populations to evolve appropriate phenotypes. A potential explanation is the swamping gene flow hypothesis, which posits that asymmetrical gene flow from large, well-adapted central populations prevents marginal populations from locally adapting. We present an empirical framework for combining gene flow, environment, and fitness-related phenotypes to infer the potential for maladaptation, and we demonstrate its application using the scarlet monkeyflower Mimulus cardinalis. We grew individuals sampled from populations on a latitudinal transect under varied temperatures and determined the phenotypic deviation (PD), the mismatch between phenotype and local environment. We inferred gene flow among populations and predicted that populations receiving the most temperature- or latitude-weighted immigration would show the greatest PD and that these populations were likely marginal. We found asymmetrical gene flow from central to marginal populations. Populations with more latitude-weighted immigration had significantly greater PD but were not necessarily marginal. Gene flow may limit local adaptation in this species, but swamping gene flow is unlikely to explain its northern range limit.     

Population structure of an endangered species living in contrasted habitats: Parnassia palustris (Saxifragaceae)

In endangered species, it is critical to analyse the level at which populations interact (i.e. dispersal) as well as the levels of inbreeding and local adaptation to set up conservation policies. These parameters were investigated in the endangered species Parnassia palustris living in contrasted habitats. We analysed population structure in 14 populations of northern France for isozymes, cpDNA markers and phenotypic traits related to fitness. Within population genetic diversity and inbreeding coefficients were not correlated to population size. Populations seem not to have undergone severe recent bottleneck. Conversely to pollen migration, seed migration seems limited at a regional scale, which could prevent colonization of new sites even if suitable habitats appear. Finally, the habitat type affects neither within-population genetic diversity nor genetic and phenotypic differentiation among populations. Thus, even if unnoticed local adaptation to habitats exists, it does not influence gene flow between populations.     

Differentiation of movement behaviour in an adaptively diverging salamander population

Dispersal is considered to be a species‐specific trait, but intraspecific variation can be high. However, when and how this complex trait starts to differentiate during the divergence of species/lineages is unknown. Here, we studied the differentiation of movement behaviour in a large salamander population (Salamandra salamandra), in which individual adaptations to different habitat conditions drive the genetic divergence of this population into two subpopulations. In this system, salamanders have adapted to the deposition and development of their larvae in ephemeral ponds vs. small first‐order streams. In general, the pond habitat is characterized as a spatially and temporally highly unpredictable habitat, while streams provide more stable and predictable conditions for the development of larvae. We analysed the fine‐scale genetic distribution of larvae, and explored whether the adaptation to different larval habitat conditions has in turn also affected dispersal strategies and home range size of adult salamanders. Based on the genetic assignment of adult individuals to their respective larval habitat type, we show that pond‐adapted salamanders occupied larger home ranges, displayed long‐distance dispersal and had a higher variability of movement types than the stream‐adapted individuals. We argue that the differentiation of phenotypically plastic traits such as dispersal and movement characteristics can be a crucial component in the course of adaptation to new habitat conditions, thereby promoting the genetic divergence of populations.     

Population genetic consequences of geographic disjunction: a prairie plant isolated on Great Lakes alvars

Species may often exhibit geographic variation in population genetic structure due to contemporary and historical variation in population size and gene flow. Here, we test the predictions that populations on the margins of a species' distribution contain less genetic variation and are more differentiated than populations towards the core of the range by comparing patterns of genetic variation at five microsatellite loci between disjunct and core populations of the perennial, allohexaploid herb Geum triflorum. We sampled nine populations isolated on alvar habitat within the eastern Great Lakes region in North America, habitats that include disjunct populations of several plant species, and compared these to 16 populations sampled from prairie habitat throughout the core of the species' distribution in midwestern Canada and the USA. Alvar populations exhibited much lower within-population diversity and contained only a subset of alleles found in prairie populations. We detected isolation by distance across the species' range and within alvar and prairie regions separately. As predicted, genetic differentiation was higher among alvar populations than among prairie populations, even after controlling for the geographic distance between sampled populations. Low diversity and high differentiation can be accounted for by the greater contemporary spatial isolation of alvar populations. However, the genetic structure of alvar populations may also have been influenced by postglacial range expansion and contraction. Our results are consistent with alvar populations being founded during an expansion of prairie habitat during the warmer, hypsithermal period approximately 5000 bp and subsequently becoming stranded on isolated alvar habitat as the climate grew cooler and wetter.