Locally-adapted Populations Research Articles

Understanding species limits through the formation of phylogeographic lineages.

The outcomes of speciation across organismal dimensions (e.g., ecological, genetic, phenotypic) are often assessed using phylogeographic methods. At one extreme, reproductively isolated lineages represent easily delimitable species differing in many or all dimensions, and at the other, geographically distinct genetic segments introgress across broad environmental gradients with limited phenotypic disparity. In the ambiguous gray zone of speciation, where lineages are genetically delimitable but still interacting ecologically, it is expected that these lineages represent species in the context of ontology and the evolutionary species concept when they are maintained over time with geographically well-defined hybrid zones, particularly at the intersection of distinct environments. As a result, genetic structure is correlated with environmental differences and not space alone, and a subset of genes fail to introgress across these zones as underlying genomic differences accumulate. We present a set of tests that synthesize species delimitation with the speciation process. We can thereby assess historical demographics and diversification processes while understanding how lineages are maintained through space and time by exploring spatial and genome clines, genotype-environment interactions, and genome scans for selected loci. Employing these tests in eight lineage-pairs of snakes in North America, we show that six pairs represent 12 "good" species and that two pairs represent local adaptation and regional population structure. The distinct species pairs all have the signature of divergence before or near the mid-Pleistocene, often with low migration, stable hybrid zones of varying size, and a subset of loci showing selection on alleles at the hybrid zone corresponding to transitions between distinct ecoregions. Locally adapted populations are younger, exhibit higher migration, and less ecological differentiation. Our results demonstrate that interacting lineages can be delimited using phylogeographic and population genetic methods that properly integrate spatial, temporal, and environmental data.

Sexual imprinting leads to speciation in locally adapted populations.

Sexual imprinting is widespread in birds and other species but its existence requires explanation. Our results suggest that sexual imprinting leads to speciation in locally-adapted populations if a neutral mating cue-e.g., novel plumage coloration-arises through mutation. Importantly, the mating cue locus is not linked to adaptation loci. Local adaptation is a necessary precursor to speciation and occurs when evolution results in stable genetic polymorphisms with one allele predominating in some areas while others predominate elsewhere. Here we use a deterministic two-niche population genetic model to map the set of migration and selection rates for which polymorphic evolutionary outcomes, i.e., local adaptations, can occur. Approximate equations for the boundaries of the set of polymorphic evolutionary outcomes were derived by Bulmer (American Naturalist, 106, 254, 1972), but our results, obtained by deterministic simulation of the evolutionary process, show that one of Bulmer's equations is inaccurate except when the level of dominance is 0.5, and fails if one of the alleles is dominant. Having an accurate map of the set of migration and selection rates for which polymorphic evolutionary outcomes can occur, we then show using the model of Sibly et al. (Ecology and Evolution, 9, 13506, 2019) that local adaptation in all analyzed cases leads to speciation if a new neutral mating cue arises by mutation. We finish by considering how genome sequencing makes possible testing our model and its predictions.

Seascape genomics of common dolphins (Delphinus delphis) reveals adaptive diversity linked to regional and local oceanography

BackgroundHigh levels of standing genomic variation in wide-ranging marine species may enhance prospects for their long-term persistence. Patterns of connectivity and adaptation in such species are often thought to be influenced by spatial factors, environmental heterogeneity, and oceanographic and geomorphological features. Population-level studies that analytically integrate genome-wide data with environmental information (i.e., seascape genomics) have the potential to inform the spatial distribution of adaptive diversity in wide-ranging marine species, such as many marine mammals. We assessed genotype-environment associations (GEAs) in 214 common dolphins (Delphinus delphis) along > 3000 km of the southern coast of Australia.ResultsWe identified 747 candidate adaptive SNPs out of a filtered panel of 17,327 SNPs, and five putatively locally-adapted populations with high levels of standing genomic variation were disclosed along environmentally heterogeneous coasts. Current velocity, sea surface temperature, salinity, and primary productivity were the key environmental variables associated with genomic variation. These environmental variables are in turn related to three main oceanographic phenomena that are likely affecting the dispersal of common dolphins: (1) regional oceanographic circulation, (2) localised and seasonal upwellings, and (3) seasonal on-shelf circulation in protected coastal habitats. Signals of selection at exonic gene regions suggest that adaptive divergence is related to important metabolic traits.ConclusionTo the best of our knowledge, this represents the first seascape genomics study for common dolphins (genus Delphinus). Information from the associations between populations and their environment can assist population management in forecasting the adaptive capacity of common dolphins to climate change and other anthropogenic impacts.

The proximate sources of genetic variation in body size plasticity: The relative contributions of feeding behaviour and development in Drosophila melanogaster

Body size is a key life-history trait that influences many aspects of an animal’s biology and is shaped by a variety of factors, both genetic and environmental. While we know that locally-adapted populations differ in the extent to which body size responds plastically to environmental conditions like diet, we have a limited understanding of what causes these differences. We hypothesized that populations could differ in the way body size responds to nutrition either by modulating growth rate, development time, feeding rate, or a combination of the above. Using three locally-adapted populations of Drosophila melanogaster from along the east coast of Australia, we investigated body size plasticity across five different diets. We then assessed how these populations differed in feeding behaviour and developmental timing on each of the diets. We observed population-specific plastic responses to nutrition for body size and feeding rate, but not development time. However, differences in feeding rate did not fully explain the differences in the way body size responded to diet. Thus, we conclude that body size variation in locally-adapted populations is shaped by a combination of growth rate and feeding behaviour. This paves the way for further studies that explore how differences in the regulation of the genetic pathways that control feeding behaviour and growth rate contribute to population-specific responses of body size to diet.

Countergradient Variation in Reptiles: Thermal Sensitivity of Developmental and Metabolic Rates Across Locally Adapted Populations.

Environmental temperature is a key driver of variation in developmental physiological rates in reptiles. Cooler temperatures extend development time and can increase the amount of energy required to achieve hatching success, which can pose fitness consequences later in life. Yet, for locally-adapted populations, genetic variation can oppose environmental variation across ecological gradients, known as countergradient variation (CnGV). Biologists often seek to understand the presence of phenotypic variation, yet the absence of such variation across environmental gradients can also reveal insights into the mechanisms underlying local adaptation. While evidence for genetic variation opposing environmental variation in physiological rates has been summarized in other taxa, the generality of CnGV variation in reptiles is yet unknown. Here I present a summary of studies measuring development time and metabolic rates in locally-adapted populations across thermal clines for 15 species of reptiles across 8 families. CnGV in development time is found to be common, while no clear pattern emerges for the thermal sensitivity of metabolic rates across locally-adapted populations. CnGV in development time may be an adaptive response in order to decrease the costly development in cool climates, however, empirical work is needed to disentangle plastic from genetic responses, and to uncover potentially general mechanisms of local thermal adaptation in reptiles.

Effect of population, collection year, after-ripening and incubation condition on seed germination of Stipa bungeana

Knowledge of the germination behavior of different populations of a species can be useful in the selection of appropriate seed sources for restoration. The aim of this study was to test the effect of seed population, collection year, after-ripening and incubation conditions on seed dormancy and germination of Stipa bungeana, a perennial grass used for revegetation of degraded grasslands on the Loess Plateau, China. Fresh S. bungeana seeds were collected from eight locally-adapted populations in 2015 and 2016. Dormancy and germination characteristics of fresh and 6-month-old dry-stored seeds were determined by incubating them over a range of alternating temperature regimes in light. Effect of water stress on germination was tested for fresh and 6-month-old dry-stored seeds. Seed dormancy and germination of S. bungeana differed with population and collection year. Six months of dry storage broke seed dormancy, broadened the temperature range for germination and increased among-population differences in germination percentage. The rank order of germination was not consistent in all germination tests, and it varied among populations. Thus, studies on comparing seed dormancy and germination among populations must consider year of collection, seed dormancy states and germination test conditions when selecting seeds for grassland restoration and management.

Does personality affect premating isolation between locally-adapted populations?

BackgroundOne aspect of premating isolation between diverging, locally-adapted population pairs is female mate choice for resident over alien male phenotypes. Mating preferences often show considerable individual variation, and whether or not certain individuals are more likely to contribute to population interbreeding remains to be studied. In the Poecilia mexicana-species complex different ecotypes have adapted to hydrogen sulfide (H2S)-toxic springs, and females from adjacent non-sulfidic habitats prefer resident over sulfide-adapted males. We asked if consistent individual differences in behavioral tendencies (animal personality) predict the strength and direction of the mate choice component of premating isolation in this system.ResultsWe characterized focal females for their personality and found behavioral measures of ‘novel object exploration’, ‘boldness’ and ‘activity in an unknown area’ to be highly repeatable. Furthermore, the interaction term between our measures of exploration and boldness affected focal females’ strength of preference (SOP) for the resident male phenotype in dichotomous association preference tests. High exploration tendencies were coupled with stronger SOPs for resident over alien mating partners in bold, but not shy, females. Shy and/or little explorative females had an increased likelihood of preferring the non-resident phenotype and thus, are more likely to contribute to rare population hybridization. When we offered large vs. small conspecific stimulus males instead, less explorative females showed stronger preferences for large male body size. However, this effect disappeared when the size difference between the stimulus males was small.ConclusionsOur results suggest that personality affects female mate choice in a very nuanced fashion. Hence, population differences in the distribution of personality types could be facilitating or impeding reproductive isolation between diverging populations depending on the study system and the male trait(s) upon which females base their mating decisions, respectively.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0712-2) contains supplementary material, which is available to authorized users.

Biotic and Climatic Velocity Identify Contrasting Areas of Vulnerability to Climate Change

Metrics that synthesize the complex effects of climate change are essential tools for mapping future threats to biodiversity and predicting which species are likely to adapt in place to new climatic conditions, disperse and establish in areas with newly suitable climate, or face the prospect of extirpation. The most commonly used of such metrics is the velocity of climate change, which estimates the speed at which species must migrate over the earth’s surface to maintain constant climatic conditions. However, “analog-based” velocities, which represent the actual distance to where analogous climates will be found in the future, may provide contrasting results to the more common form of velocity based on local climate gradients. Additionally, whereas climatic velocity reflects the exposure of organisms to climate change, resultant biotic effects are dependent on the sensitivity of individual species as reflected in part by their climatic niche width. This has motivated development of biotic velocity, a metric which uses data on projected species range shifts to estimate the velocity at which species must move to track their climatic niche. We calculated climatic and biotic velocity for the Western Hemisphere for 1961–2100, and applied the results to example ecological and conservation planning questions, to demonstrate the potential of such analog-based metrics to provide information on broad-scale patterns of exposure and sensitivity. Geographic patterns of biotic velocity for 2954 species of birds, mammals, and amphibians differed from climatic velocity in north temperate and boreal regions. However, both biotic and climatic velocities were greatest at low latitudes, implying that threats to equatorial species arise from both the future magnitude of climatic velocities and the narrow climatic tolerances of species in these regions, which currently experience low seasonal and interannual climatic variability. Biotic and climatic velocity, by approximating lower and upper bounds on migration rates, can inform conservation of species and locally-adapted populations, respectively, and in combination with backward velocity, a function of distance to a source of colonizers adapted to a site’s future climate, can facilitate conservation of diversity at multiple scales in the face of climate change.

The role of forest genetic resources in responding to biotic and abiotic factors in the context of anthropogenic climate change

The current distribution of forest genetic resources on Earth is the result of a combination of natural processes and human actions. Over time, tree populations have become adapted to their habitats including the local ecological disturbances they face. As the planet enters a phase of human-induced climate change of unprecedented speed and magnitude, however, previously locally-adapted populations are rendered less suitable for new conditions, and ‘natural’ biotic and abiotic disturbances are taken outside their historic distribution, frequency and intensity ranges. Tree populations rely on phenotypic plasticity to survive in extant locations, on genetic adaptation to modify their local phenotypic optimum or on migration to new suitable environmental conditions. The rate of required change, however, may outpace the ability to respond, and tree species and populations may become locally extinct after specific, but as yet unknown and unquantified, tipping points are reached. Here, we review the importance of forest genetic resources as a source of evolutionary potential for adaptation to changes in climate and other ecological factors. We particularly consider climate-related responses in the context of linkages to disturbances such as pests, diseases and fire, and associated feedback loops. The importance of management strategies to conserve evolutionary potential is emphasised and recommendations for policy-makers are provided.

Common Garden Experiment Reveals Genetic Control of Phenotypic Divergence between Swamp Sparrow Subspecies That Lack Divergence in Neutral Genotypes

BackgroundAdaptive divergence between populations in the face of strong selection on key traits can lead to morphological divergence between populations without concomitant divergence in neutral DNA. Thus, the practice of identifying genetically distinct populations based on divergence in neutral DNA may lead to a taxonomy that ignores evolutionarily important, rapidly evolving, locally-adapted populations. Providing evidence for a genetic basis of morphological divergence between rapidly evolving populations that lack divergence in selectively neutral DNA will not only inform conservation efforts but also provide insight into the mechanisms of the early processes of speciation. The coastal plain swamp sparrow, a recent colonist of tidal marsh habitat, differs from conspecific populations in a variety of phenotypic traits yet remains undifferentiated in neutral DNA.Methods and Principal FindingsHere we use an experimental approach to demonstrate that phenotypic divergence between ecologically separated populations of swamp sparrows is the result of local adaptation despite the lack of divergence in neutral DNA. We find that morphological (bill size and plumage coloration) and life history (reproductive effort) differences observed between wild populations were maintained in laboratory raised individuals suggesting genetic divergence of fitness related traits.Conclusions and SignificanceOur results support the hypothesis that phenotypic divergence in swamps sparrows is the result of genetic differentiation, and demonstrate that adaptive traits have evolved more rapidly than neutral DNA in these ecologically divergent populations that may be in the early stages of speciation. Thus, identifying evolutionarily important populations based on divergence in selectively neutral DNA could miss an important level of biodiversity and mislead conservation efforts.