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The future of biocontrol in the Anthropocene: A review of climate change impacts on biocontrol agents and their hosts

Biological control, the practice of using one species (biocontrol agent) to control the population of another (a host or prey species, hereafter target), can be a successful method to reduce pest species in agricultural and natural systems worldwide. Successful biocontrol agents often share a deep evolutionary history with their targets that results in high target specificity and synchronized phenology. However, with rapidly changing climatic conditions, users of biocontrol agents have questioned how climate change will affect both well-established and more recent biological control relationships. Using a meta-analysis of data collected from a systematic literature review, we evaluated the evidence for the impact of changing temperatures on the efficacy of biocontrol agents and corresponding responses in their targets. Overall, most studies of climate change impacts on biocontrol agents take place in the laboratory and focus on arthropod agents that are parasitoids. Results from our meta-analysis reveal that changes in temperature are projected to impact biocontrol agents and their targets similarly, with no overall significant changes to biocontrol agent or target performance. However, our results also show that temperature responses vary widely across study systems, as illustrated by case studies showing both positive, neutral, and negative effects of temperature on biocontrol agent efficacy, as well as variation in responses across the three core biological control measures of success: survival, reproduction, and efficacy. Our work highlights important knowledge gaps including how climate change will affect both biocontrol agents and their targets simultaneously. Additionally, we find that most current studies of climate impacts examined temperature relationships, predominantly of agricultural biocontrol agents. Increasing the breadth of studies is crucial for understanding the potential for climate change to affect the success of current and future biological control programs.

Ecological Applications

Heightened exposure to parasites favors the evolution of immunity in brood parasitic cowbirds

Immunologists and evolutionary biologists are interested in how the immune system evolves to fit an ecological niche. We studied the relationship between exposure to parasites and strength of immunity by investigating the response of two species of New World cowbirds (genus Molothrus , Icteridae), obligate brood parasites with contrasting life history strategies, to experimental arboviral infection. The South American shiny cowbird ( M. bonariensis ) is an extreme host - generalist that lays its eggs in the nests of >225 different avian species. The Central American bronzed cowbird ( M. aeneus ) is a relative host - specialist that lays its eggs preferentially in the nests of approximately 12 orioles in a single sister genus. West Nile virus provided a strong challenge and delineated immune differences between these species. The extreme host-generalist shiny cowbird, like the North American host-generalist, the brown-headed cowbird, showed significantly lower viremia to three arboviruses than related icterid species that were not brood parasites. The bronzed cowbird showed intermediate viremia. These findings support the interpretation that repeated exposure to a high diversity of parasites favors the evolution of enhanced immunity in brood parasitic cowbirds and makes them useful models for future studies of innate immunity.

Evolutionary Biology

Ecological and evolutionary conditions for fruit abortion to regulate pollinating seed-eaters and increase plant production

Coevolved mutualisms, such as those between senita cacti, yuccas, and their respective obligate pollinators, benefit both species involved in the interaction. However, in these pollination mutualisms the pollinator's larvae impose a cost on plants through consumption of developing seeds and fruit. The effects of pollinators on benefits and costs are expected to vary with the abundance of pollinators, because large population sizes result in more eggs and larval seed-eaters. Here, we develop the hypothesis that fruit abortion, which is common in yucca, senita, and plants in general, could in some cases have the function of limiting pollinator abundance and, thereby, increasing fruit production. Using a general steady-state model of fruit production and pollinator dynamics, we demonstrate that plants involved in pollinating seed-eater mutualisms can increase their fecundity by randomly aborting fruit. We show that the ecological conditions under which fruit abortion can improve plants fecundity are not unusual. They are best met when the plant is long-lived, the population dynamics of the pollinator are much faster than those of the plant, the loss of one fruit via abortion kills a larva that would have the expectation of destroying more than one fruit through its future egg laying as an adult moth, and the effects of fruit abortion on pollinator abundance are spatially localized. We then use the approach of adaptive dynamics to find conditions under which a fruit abortion strategy based on regulating the pollinator population could feasibly evolve in this type of plant–pollinator interaction.

Theoretical Population Biology

Ecological and evolutionary patterns of freshwater maturation in Pacific and Atlantic salmonines

Reproductive tactics and migratory strategies in Pacific and Atlantic salmonines are inextricably linked through the effects of migration (or lack thereof) on age and size at maturity. In this review, we focus on the ecological and evolutionary patterns of freshwater maturation in salmonines, a key process resulting in the diversification of their life histories. We demonstrate that the energetics of maturation and reproduction provides a unifying theme for understanding both the proximate and ultimate causes of variation in reproductive schedules among species, populations, and the sexes. We use probabilistic maturation reaction norms to illustrate how variation in individual condition, in terms of body size, growth rate, and lipid storage, influences the timing of maturation. This useful framework integrates both genetic and environmental contributions to conditional strategies for maturation and, in doing so, demonstrates how flexible life histories can be both heritable and subject to strong environmental influences. We review evidence that the propensity for freshwater maturation in partially anadromous species is predictable across environmental gradients at geographic and local spatial scales. We note that growth is commonly associated with the propensity for freshwater maturation, but that life-history responses to changes in growth caused by temperature may be strikingly different than changes caused by differences in food availability. We conclude by exploring how contemporary management actions can constrain or promote the diversity of maturation phenotypes in Pacific and Atlantic salmonines and caution against underestimating the role of freshwater maturing forms in maintaining the resiliency of these iconic species.

Reviews in Fish Biology and Fisheries

Parallel signatures of selection at genomic islands of divergence and the major histocompatibility complex in ecotypes of sockeye salmon across Alaska

Understanding the genetic mechanisms that facilitate adaptive radiation is an important component of evolutionary biology. Here, we genotyped 82 neutral SNPs, seven SNPs in islands of divergence identified in a previous study (island SNPs), and a region of the major histocompatibility complex (MHC) in 32 populations of sockeye salmon to investigate whether conserved genes and genomic regions are involved in adaptive radiation. Populations representing three ecotypes were sampled from seven drainages with differing habitats and colonization histories spanning a range of 2,000 km. We found strong signatures of parallel selection across drainages at the island SNPs and MHC, suggesting that the same loci undergo divergent selection during adaptive radiation. However, patterns of differentiation at most island SNPs and the MHC were not associated with ecotypes, suggesting that these loci are responding differently to a mosaic of selective pressures. Our study provides some of the first evidence that conserved genomic islands may be involved in adaptive divergence of salmon populations. Additionally, our data provide further support for the hypothesis that sockeye salmon inhabiting rivers unconnected to lakes harbour similar genetic diversity across large distances, are likely the ancestral form of the species, and have repeatedly recolonized lake systems as they have become available after glacial recession. Finally, our results highlight the value and importance of validating outlier loci by screening additional populations and regions, a practice that will hopefully become more common in the future.

Alaska

Movement beyond the mean: decoupling sources of individual variation in brook trout movement across seasons

Movement is an important eco-evolutionary process that can shape population and ecosystem structure and function. Accordingly, a firm understanding of species movement ecology is often foundational to effective management and conservation. However, despite movement being an inherently individual-level behavior, there remains a tendency to describe dispersal and migration patterns using simple population-level processes and effects. Overlooking within- and among-individual variation in movement risks incomplete understanding of the intrinsic and extrinsic factors that govern dispersal dynamics and could potentially result in inadequate management of critical behavioral phenotypes. In this study, we monitored movement of over 100 brook trout ( Salvelinus fontinalis ) and quantified the effect of individual-level traits, season, and their interactions to better understand factors that influence vagility. Our results suggest that movement was higher in fall than in summer, particularly for fish in poor condition. But we found no significant main effects for sex, providing no evidence for sex-biased dispersal. To better understand sources of individual variation, we also allowed for sex- and season-specific residual standard deviations. In doing so, we found that, on average, movement was more variable in fall compared to summer, and that females were more variable than males in vagility. Taken together, these results demonstrate how intrinsic, individual-level traits can interact with abiotic environmental conditions to determine movement. They also highlight the potential for simple explanations of movement ecology to overlook important traits that may help predict individual-level behaviors.

Pennsylvania

Vive la résistance: genome-wide selection against introduced alleles in invasive hybrid zones

Evolutionary and ecological consequences of hybridization between native and invasive species are notoriously complicated because patterns of selection acting on non-native alleles can vary throughout the genome and across environments. Rapid advances in genomics now make it feasible to assess locus-specific and genome-wide patterns of natural selection acting on invasive introgression within and among natural populations occupying diverse environments. We quantified genome-wide patterns of admixture across multiple independent hybrid zones of native westslope cutthroat trout and invasive rainbow trout, the world's most widely introduced fish, by genotyping 339 individuals from 21 populations using 9380 species-diagnostic loci. A significantly greater proportion of the genome appeared to be under selection favouring native cutthroat trout (rather than rainbow trout), and this pattern was pervasive across the genome (detected on most chromosomes). Furthermore, selection against invasive alleles was consistent across populations and environments, even in those where rainbow trout were predicted to have a selective advantage (warm environments). These data corroborate field studies showing that hybrids between these species have lower fitness than the native taxa, and show that these fitness differences are due to selection favouring many native genes distributed widely throughout the genome.

Proceedings of the Royal Society B: Biological Sci

Nutritional stress affects corticosterone deposition in feathers of Caspian tern chicks

Stressful environmental conditions affect the adrenocortical function of developing animals, which can have consequences for their fitness. Discovery of the avian stress hormone corticosterone (CORT) in feathers has the potential to broaden the application of endocrine research in ecological and evolutionary studies of wild birds by providing a long-term measure of CORT secretion. Mechanisms of CORT deposition in feathers are not well known and few studies have related feather CORT to circulating plasma CORT during feather growth. Our objective was to experimentally test the validity of using feather CORT as a measure of CORT secretion in developing birds experiencing nutritional stress. Caspian tern Hydroprogne caspia chicks were fed ad libitum or restricted (35% less than ad libitum) diets for four weeks. We measured CORT in feathers from these chicks to examine the relationship between feather CORT concentrations and nutritional limitation, circulating plasma CORT, and feather development. We found that feather CORT was higher in controls fed ad libitum than in restricted individuals, despite higher levels of plasma CORT in restricted chicks compared to controls. Feather mass and growth rates were strongly and positively related to feather CORT concentrations in both treatments. This is the first experimental study to show that feather CORT concentrations can be lower in response to nutritional stress, even when plasma CORT concentrations are elevated. Our results indicate that CORT deposition in feathers may be confounded when feather mass and growth rates are compromised by nutritional stress. We conclude that feather CORT can be used for assessing nutritional stress in growing birds, but the direction of response depends on how strongly stress affects feather development.

Journal of Avian Biology

Phylogenetic relationships within the Alcidae (Charadriiformes: Aves) inferred from total molecular evidence

The Alcidae is a unique assemblage of Northern Hemisphere seabirds that forage by "flying" underwater. Despite obvious affinities among the species, their evolutionary relationships are unclear. We analyzed nucleotide sequences of 1,045 base pairs of the mitochondrial cytochrome b gene and allelic profiles for 37 allozyme loci in all 22 extant species. Trees were constructed on independent and combined data sets using maximum parsimony and distance methods that correct for superimposed changes. Alternative methods of analysis produced only minor differences in relationships that were supported strongly by bootstrapping or standard error tests. Combining sequence and allozyme data into a single analysis provided the greatest number of relationships receiving strong support. Addition of published morphological and ecological data did not improve support for any additional relationship. All analyses grouped species into six distinct lineages: (1) the dovekie ( Alle alle ) and auks, (2) guillemots, (3) brachyramphine murrelets, (4) synthliboramphine murrelets, (5) true auklets, and (6) the rhinoceros auklet ( Cerorhinca monocerata ) and puffins. The two murres (genus Uria ) were sister taxa, and the black guillemot ( Cepphus grylle ) was basal to the other guillemots. The Asian subspecies of the marbled murrelet ( Brachyramphus marmoratus perdix ) was the most divergent brachyramphine murrelet, and two distinct lineages occurred within the synthliboramphine murrelets. Cassin's auklet ( Ptychoramphus aleuticus ) and the rhinoceros auklet were basal to the other auklets and puffins, respectively, and the Atlantic ( Fratercula arctica ) and horned ( Fratercula corniculata ) puffins were sister taxa. Several relationships among tribes, among the dovekie and auks, and among the auklets could not be resolved but resembled "star" phylogenies indicative of adaptive radiations at different depths within the trees.

Molecular Biology and Evolution

Secondary contact erodes Pleistocene diversification in a wide-ranging freshwater mussel (Quadrula)

The isolated river drainages of eastern North America serve as a natural laboratory to investigate the roles of allopatry and secondary contact in the evolutionary trajectories of recently diverged lineages. Drainage divides facilitate allopatric speciation, but due to their sensitivity to climatic and geomorphological changes, neighboring rivers frequently coalesce, creating recurrent opportunities of isolation and contact throughout the history of aquatic lineages. The freshwater mussel Quadrula quadrula is widely distributed across isolated rivers of eastern North America and possesses high phenotypic and molecular variation across its range. We integrate sequence data from three genomes, including female- and male-inherited mitochondrial markers and thousands of nuclear encoded SNPs with morphology and geography to illuminate the group's divergence history. Across contemporary isolated rivers, we found continuums of molecular and morphological variation, following a pattern of isolation by distance. In contact zones, hybridization was frequent with no apparent fitness consequences, as advanced hybrids were common. Accordingly, we recognize Q. quadrula as a single cohesive species with subspecific variation ( Q. quadrula rumphiana ). Demographic modeling and divergence dating supported a divergence history characterized by allopatric vicariance followed by secondary contact, likely driven by river rearrangements and Pleistocene glacial cycles. Despite clinal range-wide variation and hybridization in contact zones, the process-based species delimitation tool delimitR, which considers demographic scenarios like secondary contact, supported the delimitation of the maximum number of species tested. As such, when interpreting species delimitation results, we suggest careful consideration of spatial sampling and subsequent geographic patterns of biological variation, particularly for wide-ranging taxa.

eastern North America

The role of neutral and adaptive genomic variation in population diversification and speciation in two ground squirrel species of conservation concern

Understanding the neutral (demographic) and adaptive processes leading to the differentiation of species and populations is a critical component of evolutionary and conservation biology. In this context, recently diverged taxa represent a unique opportunity to study the process of genetic differentiation. Northern and southern Idaho ground squirrels ( Urocitellus brunneus —NIDGS, and U . endemicus —SIDGS, respectively) are a recently diverged pair of sister species that have undergone dramatic declines in the last 50 years and are currently found in metapopulations across restricted spatial areas with distinct environmental pressures. Here we genotyped single-nucleotide polymorphisms (SNPs) from buccal swabs with restriction site-associated DNA sequencing (RADseq). With these data we evaluated neutral genetic structure at both the inter- and intraspecific level, and identified putatively adaptive SNPs using population structure outlier detection and genotype–environment association (GEA) analyses. At the interspecific level, we detected a clear separation between NIDGS and SIDGS, and evidence for adaptive differentiation putatively linked to torpor patterns. At the intraspecific level, we found evidence of both neutral and adaptive differentiation. For NIDGS, elevation appears to be the main driver of adaptive differentiation, while neutral variation patterns match and expand information on the low connectivity between some populations identified in previous studies using microsatellite markers. For SIDGS, neutral substructure generally reflected natural geographical barriers, while adaptive variation reflected differences in land cover and temperature, as well as elevation. These results clearly highlight the roles of neutral and adaptive processes for understanding the complexity of the processes leading to species and population differentiation, which can have important conservation implications in susceptible and threatened species.

Idaho

Evolutionary history predicts high-impact invasions by herbivorous insects

A long‐standing goal of invasion biology is to identify factors driving highly variable impacts of non‐native species. Although hypotheses exist that emphasize the role of evolutionary history (e.g., enemy release hypothesis & defense‐free space hypothesis), predicting the impact of non‐native herbivorous insects has eluded scientists for over a century. Using a census of all 58 non‐native conifer‐specialist insects in North America, we quantified the contribution of over 25 factors that could affect the impact they have on their novel hosts, including insect traits (fecundity, voltinism, native range, etc.), host traits (shade tolerance, growth rate, wood density, etc.), and evolutionary relationships (between native and novel hosts and insects). We discovered that divergence times between native and novel hosts, the shade and drought tolerance of the novel host, and the presence of a coevolved congener on a shared host, were more predictive of impact than the traits of the invading insect. These factors built upon each other to strengthen our ability to predict the risk of a non‐native insect becoming invasive. This research is the first to empirically support historically assumed hypotheses about the importance of evolutionary history as a major driver of impact of non‐native herbivorous insects. Our novel, integrated model predicts whether a non‐native insect not yet present in North America will have a one in 6.5 to a one in 2,858 chance of causing widespread mortality of a conifer species if established (R2 = 0.91) Synthesis and applications. With this advancement, the risk to other conifer host species and regions can be assessed, and regulatory and pest management efforts can be more efficiently prioritized.

Ecology and Evolution

Determinants and consequences of dispersal in vertebrates with complex life cycles: a review of pond-breeding amphibians

Dispersal is a central process in ecology and evolution. It strongly influences the dynamics of spatially structured populations, by affecting population growth rate and local colonization-extinction processes. Dispersal can also influence evolutionary processes because it determines rates and patterns of gene flow in spatially structured populations and is closely linked to local adaptation. For these reasons, dispersal has received considerable attention from ecologists and evolutionary biologists. However, although it has been studied extensively in taxa such as birds and mammals, much less is known about dispersal in vertebrates with complex life cycles such as pond-breeding amphibians. Over the past two decades, researchers have taken an interest in amphibian dispersal and initiated both fundamental and applied studies, using a broad range of experimental and observational approaches. This body of research reveals complex dispersal patterns, causations and syndromes, with dramatic consequences for the demography and genetics of amphibian populations. In this review, our goals are to (1) redefine and clarify the concept of amphibian dispersal, (2) review current knowledge about the effects of individual (i.e., condition-dependent dispersal) and environmental (i.e., context-dependent dispersal) factors during the three stages of dispersal (i.e., emigration, immigration, transience), (3) identify the demographic and genetic consequences of dispersal in spatially structured amphibian populations, and (4) propose new research avenues to extend our understanding of amphibian dispersal. In particular, we emphasize the need to (1) quantify dispersal rate and distance rigorously using suitable model systems, (2) investigate the genetic basis and dispersal evolution patterns, and (3) examine dispersal-related eco-evolutionary dynamics. These proposed research avenues tap from the recent advances in quantitative and molecular methods and have the potential to improve our understanding of dispersal in organisms with complex life cycles.

The Quarterly Review of Biology

Conditions favouring Bromus tectorum dominance of endangered sagebrush steppe ecosystems

1. Ecosystem invasibility is determined by combinations of environmental variables, invader attributes, disturbance regimes, competitive abilities of resident species and evolutionary history between residents and disturbance regimes. Understanding the relative importance of each factor is critical to limiting future invasions and restoring ecosystems. 2. We investigated factors potentially controlling Bromus tectorum invasions into Artemisia tridentata ssp. wyomingensis communities across 75 sites in the Great Basin. We measured soil texture, cattle grazing intensity, gaps among perennial plants and plant cover including B. tectorum, biological soil crusts (BSCs) and bare soil. Using a priori knowledge, we developed a multivariate hypothesis of the susceptibility of Artemisia ecosystems to B. tectorum invasion and used the model to assess the relative importance of the factors driving the magnitude of such invasions. 3. Model results imply that bunchgrass community structure, abundance and composition, along with BSC cover, play important roles in controlling B. tectorum dominance. Evidence suggests abundant bunchgrasses limit invasions by limiting the size and connectivity of gaps between vegetation, and BSCs appear to limit invasions within gaps. Results also suggest that cattle grazing reduces invasion resistance by decreasing bunchgrass abundance, shifting bunchgrass composition, and thereby increasing connectivity of gaps between perennial plants while trampling further reduces resistance by reducing BSC. 4. Synthesis and applications. Grazing exacerbates Bromus tectorum dominance in one of North America's most endangered ecosystems by adversely impacting key mechanisms mediating resistance to invasion. If the goal is to conserve and restore resistance of these systems, managers should consider maintaining or restoring: (i) high bunchgrass cover and structure characterized by spatially dispersed bunchgrasses and small gaps between them; (ii) a diverse assemblage of bunchgrass species to maximize competitive interactions with B. tectorum in time and space; and (iii) biological soil crusts to limit B. tectorum establishment. Passive restoration by reducing cumulative cattle grazing may be one of the most effective means of achieving these three goals.

Journal of Applied Ecology

Genetic diversity is related to climatic variation and vulnerability in threatened bull trout

Understanding how climatic variation influences ecological and evolutionary processes is crucial for informed conservation decision-making. Nevertheless, few studies have measured how climatic variation influences genetic diversity within populations or how genetic diversity is distributed across space relative to future climatic stress. Here, we tested whether patterns of genetic diversity (allelic richness) were related to climatic variation and habitat features in 130 bull trout ( Salvelinus confluentus ) populations from 24 watersheds (i.e., ~4&ndash;7th order river subbasins) across the Columbia River Basin, USA. We then determined whether bull trout genetic diversity was related to climate vulnerability at the watershed scale, which we quantified on the basis of exposure to future climatic conditions (projected scenarios for the 2040s) and existing habitat complexity. We found a strong gradient in genetic diversity in bull trout populations across the Columbia River Basin, where populations located in the most upstream headwater areas had the greatest genetic diversity. After accounting for spatial patterns with linear mixed models, allelic richness in bull trout populations was positively related to habitat patch size and complexity, and negatively related to maximum summer temperature and the frequency of winter flooding. These relationships strongly suggest that climatic variation influences evolutionary processes in this threatened species and that genetic diversity will likely decrease due to future climate change. Vulnerability at a watershed scale was negatively correlated with average genetic diversity ( r = &minus;0.77; P < 0.001); watersheds containing populations with lower average genetic diversity generally had the lowest habitat complexity, warmest stream temperatures, and greatest frequency of winter flooding. Together, these findings have important conservation implications for bull trout and other imperiled species. Genetic diversity is already depressed where climatic vulnerability is highest; it will likely erode further in the very places where diversity may be most needed for future persistence.

Global Change Biology

Elevational speciation in action? Restricted gene flow associated with adaptive divergence across an altitudinal gradient

Evolutionary theory predicts that divergent selection pressures across elevational gradients could cause adaptive divergence and reproductive isolation in the process of ecological speciation. Although there is substantial evidence for adaptive divergence across elevation, there is less evidence that this restricts gene flow. Previous work in the boreal chorus frog (Pseudacris maculata) has demonstrated adaptive divergence in morphological, life history and physiological traits across an elevational gradient from approximately 1500&ndash;3000 m in the Colorado Front Range, USA. We tested whether this adaptive divergence is associated with restricted gene flow across elevation &ndash; as would be expected if incipient speciation were occurring &ndash; and, if so, whether behavioural isolation contributes to reproductive isolation. Our analysis of 12 microsatellite loci in 797 frogs from 53 populations revealed restricted gene flow across elevation, even after controlling for geographic distance and topography. Calls also varied significantly across elevation in dominant frequency, pulse number and pulse duration, which was partly, but not entirely, due to variation in body size and temperature across elevation. However, call variation did not result in strong behavioural isolation: in phonotaxis experiments, low-elevation females tended to prefer an average low-elevation call over a high-elevation call, and vice versa for high-elevation females, but this trend was not statistically significant. In summary, our results show that adaptive divergence across elevation restricts gene flow in P. maculata, but the mechanisms for this potential incipient speciation remain open.

Colorado

Genetic and phenotypic variation along an ecological gradient in lake trout Salvelinus namaycush

Background Adaptive radiation involving a colonizing phenotype that rapidly evolves into at least one other ecological variant, or ecotype, has been observed in a variety of freshwater fishes in post-glacial environments. However, few studies consider how phenotypic traits vary with regard to neutral genetic partitioning along ecological gradients. Here, we present the first detailed investigation of lake trout Salvelinus namaycush that considers variation as a cline rather than discriminatory among ecotypes. Genetic and phenotypic traits organized along common ecological gradients of water depth and geographic distance provide important insights into diversification processes in a lake with high levels of human disturbance from over-fishing. Results Four putative lake trout ecotypes could not be distinguished using population genetic methods, despite morphological differences. Neutral genetic partitioning in lake trout was stronger along a gradient of water depth, than by locality or ecotype. Contemporary genetic migration patterns were consistent with isolation-by-depth. Historical gene flow patterns indicated colonization from shallow to deep water. Comparison of phenotypic ( Pst ) and neutral genetic variation ( Fst ) revealed that morphological traits related to swimming performance (e.g., buoyancy, pelvic fin length) departed more strongly from neutral expectations along a depth gradient than craniofacial feeding traits. Elevated phenotypic variance with increasing water depth in pelvic fin length indicated possible ongoing character release and diversification. Finally, differences in early growth rate and asymptotic fish length across depth strata may be associated with limiting factors attributable to cold deep-water environments. Conclusion We provide evidence of reductions in gene flow and divergent natural selection associated with water depth in Lake Superior. Such information is relevant for documenting intraspecific biodiversity in the largest freshwater lake in the world for a species that recently lost considerable genetic diversity and is now in recovery. Unknown is whether observed patterns are a result of an early stage of incipient speciation, gene flow-selection equilibrium, or reverse speciation causing formerly divergent ecotypes to collapse into a single gene pool.

Lake Superior, Isle Royale

Bringing traits back in the equation: A roadmap to understand species redistribution

Ecological and evolutionary theories have proposed that species traits should be important in mediating species responses to contemporary climate change; yet, empirical evidence has so far provided mixed evidence for the role of behavioral, life history, or ecological characteristics in facilitating or hindering species range shifts. As such, the utility of trait-based approaches to predict species redistribution under climate change has been called into question. We develop the perspective, supported by evidence, that trait variation, if used carefully can have high potential utility, but that past analyses have in many cases failed to identify an explanatory value for traits by not fully embracing the complexity of species range shifts. First, we discuss the relevant theory linking species traits to range shift processes at the leading (expansion) and trailing (contraction) edges of species distributions and highlight the need to clarify the mechanistic basis of trait-based approaches. Second, we provide a brief overview of range shift–trait studies and identify new opportunities for trait integration that consider range-specific processes and intraspecific variability. Third, we explore the circumstances under which environmental and biotic context dependencies are likely to affect our ability to identify the contribution of species traits to range shift processes. Finally, we propose that revealing the role of traits in shaping species redistribution may likely require accounting for methodological variation arising from the range shift estimation process as well as addressing existing functional, geographical, and phylogenetic biases. We provide a series of considerations for more effectively integrating traits as well as extrinsic and methodological factors into species redistribution research. Together, these analytical approaches promise stronger mechanistic and predictive understanding that can help society mitigate and adapt to the effects of climate change on biodiversity.

Global Change Biology