Genetic architecture of dispersal and local adaptation drives accelerating range expansions

Contemporary evolution has the potential to significantly alter biotic responses to global change, including range expansion dynamics and biological invasions. However, predictive models often make highly simplifying assumptions about the genetic architecture underlying relevant traits. This can be problematic since genetic architecture defines evolvability, that is, evolutionary rates, and higher order evolutionary processes, which determine whether evolution will be able to keep up with environmental change or not. Therefore, we here study the impact of the genetic architecture of dispersal and local adaptation, two central traits of high relevance for range expansion dynamics, on the speed and variability of range expansions into an environmental gradient, such as temperature. In our theoretical model we assume that dispersal and local adaptation traits result from the products of two non-interacting gene-regulatory networks (GRNs). We compare our model to simpler quantitative genetics models and show that in the GRN model, range expansions are accelerated, faster and more variable. Increased variability implies that these evolutionary changes reduce predictability. We further find that acceleration in the GRN model is primarily driven by an increase in the rate of local adaptation to novel habitats which results from greater sensitivity to mutation (decreased robustness) and increased gene expression. Our results highlight how processes at microscopic scales, here, within genomes, can impact the predictions of large scale, macroscopic phenomena, such as range expansions, by modulating the rate of evolution.

Predictability and parallelism in the contemporary evolution of hybrid genomes

Hybridization between species is widespread across the tree of life. As a result, many species, including our own, harbor regions of their genome derived from hybridization. Despite the recognition that this process is widespread, we understand little about how the genome stabilizes following hybridization, and whether the mechanisms driving this stabilization tend to be shared across species. Here, we dissect the drivers of variation in local ancestry across the genome in replicated hybridization events between two species pairs of swordtail fish: Xiphophorus birchmanni × X. cortezi and X. birchmanni × X. malinche. We find surprisingly high levels of repeatability in local ancestry across the two types of hybrid populations. This repeatability is attributable in part to the fact that the recombination landscape and locations of functionally important elements play a major role in driving variation in local ancestry in both types of hybrid populations. Beyond these broad scale patterns, we identify dozens of regions of the genome where minor parent ancestry is unusually low or high across species pairs. Analysis of these regions points to shared sites under selection across species pairs, and in some cases, shared mechanisms of selection. We show that one such region is a previously unknown hybrid incompatibility that is shared across X. birchmanni × X. cortezi and X. birchmanni × X. malinche hybrid populations.

Cold tolerance varies among invasive populations of the Asian clam Corbicula fluminea

The distribution of the subtropical Asian clam Corbicula fluminea (Müller, 1774), one of the world’s most invasive freshwater molluscs, is reportedly constrained by a lower thermal tolerance limit of 2°C. Although its occurrence in north temperate regions is typically restricted to artificially heated waterbodies, the species has been found to overwinter in unheated lakes and rivers. In laboratory experiments, we compared the cold tolerance of populations from several geographically distinct sites spanning 35°N to 46°N in eastern North America. Each population contained individuals that fully recovered from two months of continuous exposure to near freezing (1°C) conditions, contrary to published accounts of C. fluminea’s thermal ecology. Survivorship increased with body size and was enhanced by prior acclimation to a low temperature (10°C) compared to a higher one (18°C). When acclimated to 10°C, clams from northern populations exhibited greater survivorship (55.0 ± 16.1%) than those from southern populations (26.7 ± 19.2%). However, one southern population demonstrated survivorship as great as that of the most tolerant northern population, suggesting that its clams could overwinter in unheated northern waterbodies. Differences among populations indicate either that contemporary evolution has occurred or that developmental plasticity shapes future acclimation responses.

Epigenetics and the success of invasive plants

Biological invasions impose ecological and economic problems on a global scale, but also provide extraordinary opportunities for studying contemporary evolution. It is critical to understand the evolutionary processes that underly invasion success in order to successfully manage existing invaders, and to prevent future invasions. As successful invasive species sometimes are suspected to rapidly adjust to their new environments in spite of very low genetic diversity, we are obliged to re-evaluate genomic-level processes that translate into phenotypic diversity. In this paper, we review work that supports the idea that trait variation, within and among invasive populations, can be created through epigenetic or other non-genetic processes, particularly in clonal invaders where somatic changes can persist indefinitely. We consider several processes that have been implicated as adaptive in invasion success, focusing on various forms of ‘genomic shock’ resulting from exposure to environmental stress, hybridization and whole-genome duplication (polyploidy), and leading to various patterns of gene expression re-programming and epigenetic changes that contribute to phenotypic variation or even novelty. These mechanisms can contribute to transgressive phenotypes, including hybrid vigour and novel traits, and may thus help to understand the huge successes of some plant invaders, especially those that are genetically impoverished. This article is part of the theme issue ‘How does epigenetics influence the course of evolution?’

Balancing selection and drift in a polymorphic salamander metapopulation

Understanding how genetic variation is maintained in a metapopulation is a longstanding problem in evolutionary biology. Historical resurveys of polymorphisms have offered efficient insights about evolutionary mechanisms, but are often conducted on single, large populations, neglecting the more comprehensive view afforded by considering all populations in a metapopulation. Here, we resurveyed a metapopulation of spotted salamanders ( Ambystoma maculatum ) to understand the evolutionary drivers of frequency variation in an egg mass colour polymorphism. We found that this metapopulation was demographically, phenotypically and environmentally stable over the last three decades. However, further analysis revealed evidence for two modes of evolution in this metapopulation—genetic drift and balancing selection. Although we cannot identify the balancing mechanism from these data, our findings present a clear view of contemporary evolution in colour morph frequency and demonstrate the importance of metapopulation-scale studies for capturing a broad range of evolutionary dynamics.

Threespine Stickleback in Lake Constance: The Ecology and Genomic Substrate of a Recent Invasion

Invasive species can be powerful models for studying contemporary evolution in natural environments. As invading organisms often encounter new habitats during colonization, they will experience novel selection pressures. Threespine stickleback (Gasterosteus aculeatus complex) have recently colonized large parts of Switzerland and are invasive in Lake Constance. Introduced to several watersheds roughly 150 years ago, they spread across the Swiss Plateau (400–800 m a.s.l.), bringing three divergent hitherto allopatric lineages into secondary contact. As stickleback have colonized a variety of different habitat types during this recent range expansion, the Swiss system is a useful model for studying contemporary evolution with and without secondary contact. For example, in the Lake Constance region there has been rapid phenotypic and genetic divergence between a lake population and some stream populations. There is considerable phenotypic variation within the lake population, with individuals foraging in and occupying littoral, offshore pelagic, and profundal waters, the latter of which is a very unusual habitat for stickleback. Furthermore, adults from the lake population can reach up to three times the size of adults from the surrounding stream populations, and are large by comparison to populations globally. Here, we review the historical origins of the threespine stickleback in Switzerland, and the ecomorphological variation and genomic basis of its invasion in Lake Constance. We also outline the potential ecological impacts of this invasion, and highlight the interest for contemporary evolution studies.

Drivers of Pine Island Glacier speed-up between 1996 and 2016

Pine Island Glacier in West Antarctica is among the fastest changing glaciers worldwide. Over the last 2 decades, the glacier has lost in excess of a trillion tons of ice, or the equivalent of 3 mm of sea level rise. The ongoing changes are thought to have been triggered by ocean-induced thinning of its floating ice shelf, grounding line retreat, and the associated reduction in buttressing forces. However, other drivers of change, such as large-scale calving and changes in ice rheology and basal slipperiness, could play a vital, yet unquantified, role in controlling the ongoing and future evolution of the glacier. In addition, recent studies have shown that mechanical properties of the bed are key to explaining the observed speed-up. Here we used a combination of the latest remote sensing datasets between 1996 and 2016, data assimilation tools, and numerical perturbation experiments to quantify the relative importance of all processes in driving the recent changes in Pine Island Glacier dynamics. We show that (1) calving and ice shelf thinning have caused a comparable reduction in ice shelf buttressing over the past 2 decades; that (2) simulated changes in ice flow over a viscously deforming bed are only compatible with observations if large and widespread changes in ice viscosity and/or basal slipperiness are taken into account; and that (3) a spatially varying, predominantly plastic bed rheology can closely reproduce observed changes in flow without marked variations in ice-internal and basal properties. Our results demonstrate that, in addition to its evolving ice thickness, calving processes and a heterogeneous bed rheology play a key role in the contemporary evolution of Pine Island Glacier.

Contemporary evolution of the viral-sensing TLR3 gene in an isolated vertebrate population

Understanding where and how genetic variation is maintained within populations is important from an evolutionary and conservation perspective. Signatures of past selection suggest that pathogen-mediated balancing selection is a key driver of immunogenetic variation, but studies tracking contemporary evolution are needed to help resolve the evolutionary forces and mechanism at play. Previous work in a bottlenecked population of Seychelles warblers (Acrocephalus sechellensis) show that functional variation has been maintained at the viral-sensing Toll-like receptor 3 (TLR3) gene. Here, we characterise evolution at this TLR3 locus over a 25-year period within the original remnant population of the Seychelles warbler, and in four other derived, contained populations. Results show a significant and consistent temporal decline in the frequency of the TLR3C allele in the original population, and that similar declines in the TLR3C allele frequency occurred in all the derived populations. Individuals (of both sexes) with the TLR3CC genotype had lower survival, and males - but not females - that carry the TLR3C allele had significantly lower lifetime reproductive success than those with only the TLR3A allele. These results indicate that positive selection, caused by an as yet unknown agent, is driving TLR3 evolution in the Seychelles warblers. No evidence of heterozygote advantage was detected. However, whether the positive selection observed is part of a longer-term pattern of balancing selection (through fluctuating selection or rare-allele advantage) cannot be resolved without tracking the TLR3C allele in the populations over an extended period of time.