A review on trade-offs at the warm and cold ends of geographical distributions.

Species' range limits are ubiquitous. This suggests that the evolution of the ecological niche is constrained in general and at the edges of distributions in particular. While there may be many ecological and genetic reasons for this phenomenon, here we focus on the potential role of trade-offs. We performed a literature search on evidence for trade-offs associated with geographical or elevational range limits. The majority of trade-offs were reported as relevant at either the cold end of species' distribution (n = 19), the warm or dry end (n = 19) or both together (n = 14). One common type of trade-off involved accelerating growth or development (27%), often at the cost of small size. Another common type involved resistance to or tolerance of climatic extremes that occur at certain periods of the year (64%), often at the cost of small size or reduced growth. Trade-offs overlapped with some of the classic trade-offs reported in life-history evolution or thermal adaptation. The results highlight several general insights about species' niches and ranges, and we outline how future research should better integrate the ecological context and test for the presence of microevolutionary trade-offs. This article is part of the theme issue 'Species' ranges in the face of changing environments (Part II)'.

European common frog (Rana temporaria) recolonized Switzerland from multiple glacial refugia in northern Italy via trans- and circum-Alpine routes.

The high mountain ranges of Western Europe had a profound effect on the biotic recolonization of Europe from glacial refugia. The Alps present a particularly interesting case because they form an absolute barrier to dispersal for most taxa, obstructing recolonization from multiple refugia in northern Italy. Here, we investigate the effect of the European Alps on the phylogeographic history of the European common frog Rana temporaria. Based on partial cytochrome b and COXI sequences from Switzerland, we find two mitochondrial lineages roughly north and south of the Alpine ridge, with contact zones between them in eastern and western Switzerland. The northern haplogroup falls within the previously identified Western European haplogroup, while the southern haplogroup is unique to Switzerland. We find that the lineages diverged ~110 kya, at approximately the onset of the last glacial glaciation; this indicates that they are from different glacial refugia. Phylogenetic analyses suggest that the northern and southern haplogroups colonized Switzerland via trans- and circum-Alpine routes from at least two separate refugia in northern Italy. Our results illustrate how a complex recolonization history of the central European Alps can arise from the semi-permeable barrier created by high mountains.

Ecological causes of fluctuating natural selection on habitat choice in an amphibian.

We estimated natural selection targeting three traits related to habitat choice in a frog (Pseudacris maculata) breeding in pools on the rocky shores of Isle Royale, Michigan, over 16 years. Our aim was to identify the form and ecological causes of annual variation in directional and correlational selection as expressed in the survival and growth of tadpoles. We found directional selection favoring early breeding, but pool choice was under weak stabilizing selection. However, the form of stabilizing selection and the position of the optimum trait value shifted among years with the severity of disturbance and the intensity of biotic interactions. In years when wave wash and pool desiccation were severe, selection shifted to favor tadpoles in habitats where these risks were less pronounced. If predatory dragonfly larvae were abundant, selection favored tadpoles in small pools where dragonflies did not occur. When intraspecific competition was strong, selection favored early broods within a broader range of pool types. The agents of selection in this study-biotic interactions and disturbance-are common to many ecological systems and frequently exhibit temporal variation; this suggests that fluctuating selection may be widespread in natural populations.

Adaptation to elevation but limited local adaptation in an amphibian.

We performed a reciprocal transplant experiment to estimate "parallel" adaptation to elevation and "unique" adaptation to local sites at the same elevation, using the frog Rana temporaria in the Swiss Alps. It is important to distinguish these two processes because they have different implications for population structure and ecological specialization. Larvae were reared from hatching to metamorphosis within enclosures installed in their pond of origin, in three foreign ponds at the same elevation, and in four ponds at different elevation (1500-2000 m higher or lower). There were two source populations from each elevation, and adults were held in a common environment for 1 year before they were crossed to produce offspring for the experiment. Fitness was a measure that integrated larval survival, development rate, and body size. Parallel adaptation to elevation was indicated by an advantage at the home elevation (11.5% fitness difference at low elevation and 47% at high elevation). This effect was stronger than that observed in most other studies, according to a survey of previous transplant experiments across elevation (N = 8 animal species and 71 plants). Unique local adaptation within elevational zones was only 0.3-0.7 times as strong as parallel adaptation, probably because gene flow is comparatively high among nearby wetlands at the same elevation. The home-elevation advantage may reduce gene flow across the elevational gradient and enable the evolution of habitat races specialized on elevation.

Demographic Processes Linked to Genetic Diversity and Positive Selection across a Species' Range.

Demography determines the strength of genetic drift, which generally reduces genetic variation and the efficacy of selection. Here, we disentangled the importance of demographic processes at a local scale (census size and mating system) and at a species-range scale (old split between population clusters, recolonization after the last glaciation cycle, and admixture) in determining within-population genomic diversity and genomic signatures of positive selection. Analyses were based on re-sequence data from 52 populations of North American Arabidopsis lyrata collected across its entire distribution. The mating system and range dynamics since the last glaciation cycle explained around 60% of the variation in genomic diversity among populations and 52% of the variation in the signature of positive selection. Diversity was lowest in selfing compared with outcrossing populations and in areas further away from glacial refugia. In parallel, reduced positive selection was found in selfing populations and in populations with a longer route of postglacial range expansion. The signature of positive selection was also reduced in populations without admixture. We conclude that recent range expansion can have a profound influence on diversity in coding and non-coding DNA, similar in magnitude to the shift toward selfing. Distribution limits may in fact be caused by reduced effective population size and compromised positive selection in recently colonized parts of the range.

Relative importance of isolation-by-environment and other determinants of gene flow in an alpine amphibian.

A pattern of population structure called isolation-by-environment (IBE) evolves when gene flow connecting populations in different habitats is lower than expected. Although IBE is widespread, there is limited information on its magnitude compared with other factors influencing gene flow. We estimated the relative importance of IBE in the frog Rana temporaria in the Swiss Alps, a geographic context in which IBE should be relatively pronounced. The environmental factor potentially causing IBE was the length of the growing season, which is highly correlated with elevation. A sample of 992 individuals from 82 breeding sites were genotyped at 1827 single-nucleotide polymorphism markers; gene flow was estimated in four ways related to FST , genetic distance, allele sharing, and distance on a population graph. Gravity modeling and random forest regression evaluated the importance of six at-site covariates, 10 between-site covariates, and geographic distance. There was broad agreement among analysis methods and measures of gene flow: isolation-by-distance (IBD) and habitat quality between sites were of highest importance, the elevation and ruggedness of the dispersal path were about half as important, and IBE was about 10-20% as important as IBD. These results combine with other evidence to suggest that population divergence across elevational gradients is underway in amphibians.

Gene Flow Limits Adaptation along Steep Environmental Gradients.

When environmental variation is spatially continuous, dispersing individuals move among nearby sites with similar habitat conditions. But as an environmental gradient becomes steeper, gene flow may connect more divergent habitats, and this is predicted to reduce the slope of the adaptive cline that evolves. We compared quantitative genetic divergence of Rana temporaria frog populations along a 2,000-m elevational gradient in eastern Switzerland (new experimental results) with divergence along a 1,550-km latitudinal gradient in Fennoscandia (previously published results). Both studies found significant countergradient variation in larval development rate (i.e., animals from cold climates developed more rapidly). The cline was weaker with elevation than with latitude. Animals collected on both gradients were genotyped at ∼2,000 single-nucleotide polymorphism markers, revealing that dispersal distance was 30% farther on the latitudinal gradient but 3.9 times greater with respect to environmental conditions on the elevational gradient. A meta-analysis of 19 experimental studies of anuran populations spanning temperature gradients revealed that countergradient variation in larval development, while significant overall, was weaker when measured on steeper gradients. These findings support the prediction that adaptive population divergence is less pronounced, and maladaptation more pervasive, on steep environmental gradients.

Predator-induced changes in the chemical defence of a vertebrate.

1. Inducible defences are ubiquitous in the animal kingdom, but little is known about facultative changes in chemical defences in response to predators, especially so in vertebrates. 2. We tested for predator-induced changes in toxin production of larval common toads (Bufo bufo), which are known to synthesize bufadienolide compounds. 3. The experiment included larvae originating from three permanent and three temporary ponds reared in the presence or absence of chemical cues of three predators: dragonfly larvae, newts or fish. 4. Tadpoles raised with chemical cues of predation risk produced higher numbers of bufadienolide compounds and larger total bufadienolide quantities than predator-naive conspecifics. Further, the increase in intensity of chemical defence was greatest in response to fish, weakest to newts and intermediate to dragonfly larvae. Tadpoles originating from temporary and permanent ponds did not differ in their baseline toxin content or in the magnitude of their induced chemical responses. 5. These results provide the first compelling evidence for predator-induced changes in chemical defence of a vertebrate that may have evolved to enhance survival under predation risk.

A Practical Guide to the Study of Distribution Limits.

Factors that limit the geographic distribution of species are broadly important in ecology and evolutionary biology, and understanding distribution limits is imperative for predicting how species will respond to environmental change. Good data indicate that factors such as dispersal limitation, small effective population size, and isolation are sometimes important. But empirical research highlights no single factor that explains the ubiquity of distribution limits. In this article, we outline a guide to tackling distribution limits that integrates established causes, such as dispersal limitation and spatial environmental heterogeneity, with understudied causes, such as mutational load and genetic or developmental integration of traits limiting niche expansion. We highlight how modeling and quantitative genetic and genomic analyses can provide insight into sources of distribution limits. Our practical guide provides a framework for considering the many factors likely to determine species distributions and how the different approaches can be integrated to predict distribution limits using eco-evolutionary modeling. The framework should also help predict distribution limits of invasive species and of species under climate change.

Accumulation of Mutational Load at the Edges of a Species Range.

Why species have geographically restricted distributions is an unresolved question in ecology and evolutionary biology. Here, we test a new explanation that mutation accumulation due to small population size or a history of range expansion can contribute to restricting distributions by reducing population growth rate at the edge. We examined genomic diversity and mutational load across the entire geographic range of the North American plant Arabidopsis lyrata, including old, isolated populations predominantly at the southern edge and regions of postglacial range expansion at the northern and southern edges. Genomic diversity in intergenic regions declined toward distribution edges and signatures of mutational load in exon regions increased. Genomic signatures of mutational load were highly linked to phenotypically expressed load, measured as reduced performance of individual plants and lower estimated rate of population growth. The geographic pattern of load and the connection between load and population growth demonstrate that mutation accumulation reduces fitness at the edge and helps restrict species' distributions.

Is bigger really better? Relative and absolute body size influence individual growth rate under competition.

Models suggest that the mechanism of competition can influence the growth advantage associated with being large (in absolute body size or relative to other individuals in the population). Large size is advantageous under interference, but disadvantageous under exploitative competition. We addressed this prediction in a laboratory experiment on Rana temporaria tadpoles competing for limited food. There were 166 target individuals spanning a 10-fold range in body mass reared for 3 days with three other individuals that were either the same size, half as large, or twice as large as the target. Relative growth rate (proportion per day) declined with size, and absolute growth rate (mass per day) reached a peak at intermediate size and declined thereafter. Tadpoles grew slowly if they were large relative to their competitors, although relative body size was less important than absolute size. As a result, size variation declined in groups that were initially composed of individuals of variable size. Thus, bigger was not better under exploitative competition. Our results help connect individual-level behavior with individual growth and the size distribution of the population.

Spatially heterogeneous selection in nature favors phenotypic plasticity in anuran larvae.

Theory holds that adaptive phenotypic plasticity evolves under spatial or temporal variation in natural selection. I tested this prediction in a classic system of predator-induced plasticity: frog tadpoles (Rana temporaria) reacting to predaceous aquatic insects. An outdoor mesocosm experiment manipulating exposure to Aeshna dragonfly larvae revealed plasticity in most characters: growth, development, behavior, and external morphology. I measured selection by placing 1927 tadpoles into enclosures within natural ponds; photographs permitted identification of the survivors six to nine days later. Fitness was defined as a linear combination of growth, development, and survival that correlates with survival to age 2 in another anuran species. In enclosures with many predators, selection-favored character values similar to those induced by exposure to Aeshna in mesocosms. The shift in selection along the predation gradient was strongest for characters that exhibited high predator-induced plasticity. A field survey of 50 ponds revealed that predator density changes over a spatial scale relevant for movement of individual adults and larvae: 17% of variation in predation risk was among ponds separated by tens to thousands of meters and 81% was among sites ≤10 m apart within ponds. These results on heterogeneity in the selection regime confirm a key tenant of the standard model for the evolution of plasticity.

Quantitative Genetic Architecture at Latitudinal Range Boundaries: Reduced Variation but Higher Trait Independence.

Species distribution limits are hypothesized to be caused by small population size and limited genetic variation in ecologically relevant traits, but earlier studies have not evaluated genetic variation in multivariate phenotypes. We asked whether populations at the latitudinal edges of the distribution have altered quantitative genetic architecture of ecologically relevant traits compared with midlatitude populations. We calculated measures of evolutionary potential in nine Arabidopsis lyrata populations spanning the latitudinal range of the species in eastern and midwestern North America. Environments at the latitudinal extremes have reduced water availability, and therefore plants were assessed under wet and dry treatments. We estimated genetic variance-covariance (G-) matrices for 10 traits related to size, development, and water balance. Populations at southern and northern distribution edges had reduced levels of genetic variation across traits, but their G-matrices were more spherical; G-matrix orientation was unrelated to latitude. As a consequence, the predicted short-term response to selection was at least as strong in edge populations as in central populations. These results are consistent with genetic drift eroding variation and reducing the effectiveness of correlational selection at distribution margins. We conclude that genetic variation of isolated traits poorly predicts the capacity to evolve in response to multivariate selection and that the response to selection may frequently be greater than expected at species distribution margins because of genetic drift.

The relative importance of prey-borne and predator-borne chemical cues for inducible antipredator responses in tadpoles.

Chemical cues that evoke anti-predator developmental changes have received considerable attention, but it is not known to what extent prey use information from the smell of predators and from cues released through digestion. We conducted an experiment to determine the importance of various types of cues for the adjustment of anti-predator defences. We exposed tadpoles (common frog, Rana temporaria) to water originating from predators (caged dragonfly larvae, Aeshna cyanea) that were fed different types and quantities of prey outside of tadpole-rearing containers. Variation among treatments in the magnitude of morphological and behavioural responses was highly consistent. Our results demonstrate that tadpoles can assess the threat posed by predators through digestion-released, prey-borne cues and continually released predator-borne cues. These cues may play an important role in the fine-tuning of anti-predator responses and significantly affect the outcome of interactions between predators and prey in aquatic ecosystems. There has been much confusion regards terminology used in the literature, and therefore we also propose a more precise and consistent binomial nomenclature based on the timing of chemical cue release (stress-, attack-, capture-, digestion- or continually released cues) and the origin of cues (prey-borne or predator-borne cues). We hope that this new nomenclature will improve comparisons among studies on this topic.

Isocline analysis of competition predicts stable coexistence of two amphibians.

We investigated the interaction between larvae of two anuran amphibian species (Rana temporaria and Bufo bufo) to test models of two-species competition. The study had a response surface experimental design with four replicates, each consisting of 24 density combinations. Larval performance-and, by assumption, change in population size-was defined by a linear combination of survival, growth, and development. We fit six competition models from the literature and discovered that density dependence was strongly non-linear, with the highest support for the Hassel-Comins model. Rana temporaria was competitively superior to B. bufo; the impacts of both species on growth and development were about five- to tenfold greater than those on survival. Isocline analysis predicted a stable configuration, which agrees with the observation that these two species are syntopic in nature. The results of this study confirm competition theory by identifying a model structure that agrees with data and making predictions that are broadly supportive of the observations.

Non-interactive multiple predator effects on tadpole survival.

Interactions among and within three species of predators were estimated in terms of their effects on prey survival using short-term predation experiments. The prey were tadpoles (Rana temporaria), and the predators were dragonfly larvae (Anax imperator), newts (Triturus alpestris), and backswimmers (Notonecta glauca). Mortality rate per predator imposed by Triturus and Notonecta did not decline with predator density, whereas the predation rate of Anax was strongly reduced when the number of predator individuals increased. Impacts of all three predators were not altered by the presence of other species in pairwise combinations. This system is therefore characterized by interference between individual dragonflies but relatively independent effects of predator species. These results were largely predictable based on the natural history of the predators and are encouraging for attempts to model communities as assemblages of interacting species.

Predator-induced changes in metabolism cannot explain the growth/predation risk tradeoff.

Defence against predators is usually accompanied by declining rates of growth or development. The classical growth/predation risk tradeoff assumes reduced activity as the cause of these declines. However, in many cases these costs cannot be explained by reduced foraging effort or enhanced allocation to defensive structures under predation risk. Here, we tested for a physiological origin of defence costs by measuring oxygen consumption in tadpoles (Rana temporaria) exposed to predation risk over short and long periods of time. The short term reaction was an increase in oxygen consumption, consistent with the "fight-or-flight" response observed in many organisms. The long term reaction showed the opposite pattern: tadpoles reduced oxygen consumption after three weeks exposure to predators, which would act to reduce the growth cost of predator defence. The results point to an instantaneous and reversible stress response to predation risk. This suggests that the tradeoff between avoiding predators and growing rapidly is not caused by changes in metabolic rate, and must be sought in other behavioural or physiological processes.

Body size, competitive interactions, and the local distribution of Triturus newts.

1. Pairs of European Triturus newt species of similar size tend not to co-occur syntopically, suggesting that similarity in body size is associated with competitive interactions that prevent coexistence. I tested this hypothesis with an experiment involving larvae of four species in 675-L artificial ponds. 2. There were strong interactions between most species pairs. Even the small T. helveticus had a clear impact on the larger T. alpestris. Pairs of species with different body sizes did not interact less strongly. 3. A standard increase in competitor biomass (c. 2 g mass at metamorphosis) caused 42% lower expected survival from hatching to 1 year of age, regardless of whether the species were of similar or different size. In most cases this resulted from delayed metamorphosis, reduced size at emergence, and slightly lower larval survival. 4. A standard increase in competitor density (0.74 individuals m(-2)) caused a greater reduction in expected 1-year survival when the competitor was larger (18% decline) than when both species were of similar size (6% decline), primarily because the very large T. cristatus consumed the smallest species. 5. These findings suggest that species interactions during the larval stage cannot explain distribution patterns of same- and different-sized Triturus.

The change in quantitative genetic variation with inbreeding.

Inbreeding is known to reduce heterozygosity of neutral genetic markers, but its impact on quantitative genetic variation is debated. Theory predicts a linear decline in additive genetic variance (V(A)) with increasing inbreeding coefficient (F) when loci underlying the trait act additively, but a nonlinear hump-shaped relationship when dominance and epistasis are important. Predictions for heritability (h2) are similar, although the exact shape depends on the value of h2 in the absence of inbreeding. We located 22 published studies in which the level of genetic variation in experimentally inbred populations (measured by V(A) or h2) was compared with that in outbred control populations. For life-history traits, the data strongly supported a nonlinear change in genetic variation with increasing F. V(A) and h2 were, respectively, 244% and 50% higher at F = 0.4 than in outbred populations, and dominance plus epistatic variance together exceeded additive variance by a factor of four. For nonfitness traits the decline was linear and estimates of nonadditive variance were small. These results confirm that population bottlenecks frequently increase V(A) in some traits, and imply that life-history traits are underlain by substantial dominance or epistasis. However, the importance of drift-induced genetic variation in conservation or evolutionary biology is questionable, in part because inbreeding depression usually accompanies inbreeding.

Genomic compatibility occurs over a wide range of parental genetic similarity in an outcrossing plant.

The theory of inbreeding and outbreeding suggests that there is a hump-shaped relationship between the genetic similarity of sexually reproducing parents and the performance of their offspring. Inbreeding depression occurs when genetic similarity is high, whereas hybrid breakdown is expected when genetic similarity is low. Between these extremes, the effect of genetic similarity on fitness is unclear. We studied the shape of this relationship by crossing 65 target genotypes of the clonal, self-incompatible Ranunculus reptans with partner genotypes spanning a broad scale of genetic similarity, ranging from crosses within populations to between-population crosses and hybridisation with a closely related species. Offspring were raised in outdoor tubs. Results revealed a quadratic relationship between parental genetic distance and offspring performance, with the clonal component of fitness more strongly hump-shaped than the sexual component. Optimal genetic similarity encompassed a broad range of within-population and between-population crosses. This pattern of genomic compatibility has important implications for the evolution of mating systems and mate choice.