Natural selection in the origin: how does selection act on snails’ shell colour in the source of a diversified population?

The mechanisms of adaptive radiation with phenotypic diversification and further adaptive speciation have been becoming clearer through a number of studies. Natural selection is one of the primary factors that contribute to these mechanisms. It has been demonstrated that divergent natural selection acts on a certain trait in adaptive radiation. However, it is not often known how natural selection acts on the source of a diversified population, although it has been detected in phylogenetic studies. Our study demonstrates how selection acts on a trait in a source population of diversified population using the Japanese land snail Euhadra peliomphala simodae. This snail’s shell colour has diversified due to disruptive selection after migration from the mainland to islands. We used trail-camera traps to identify the cause of natural selection on both the mainland and an island. We then conducted a mark-recapture experiment on the mainland to detect natural selection and compare the shape and strength of it to previous study in an island. In total, we captured and marked around 1,700 snails, and some of them were preyed on by an unknown predator. The trail-camera traps showed that the predator is the large Japanese field mouse Apodemus speciosus, but this predation did not correlate with shell colour. A Bayesian approach showed that the stabilising selection from factors other than predation acted on shell colour. Our results suggest that natural selection was changed by migration, which could explain the ultimate cause of phenotypic diversification in adaptive radiation that was not due to predation.

Assortative mating, sexual selection and their consequences for gene flow in Littorina

When divergent populations are connected by gene flow, the establishment of complete reproductive isolation usually requires the joint action of multiple barrier effects. One example where multiple barrier effects are coupled consists of a single trait that is under divergent natural selection and also mediates assortative mating. Such multiple-effect traits can strongly reduce gene flow. However, there are few cases where patterns of assortative mating have been described quantitatively and their impact on gene flow has been determined. Two ecotypes of the coastal marine snail, Littorina saxatilis, occur in North Atlantic rocky-shore habitats dominated by either crab predation or wave action. There is evidence for divergent natural selection acting on size, and size-assortative mating has previously been documented. Here, we analyze the mating pattern in L. saxatilis with respect to size in intensively-sampled transects across boundaries between the habitats. We show that the mating pattern is mostly conserved between ecotypes and that it generates both assortment and directional sexual selection for small male size. Using simulations, we show that the mating pattern can contribute to reproductive isolation between ecotypes but the barrier to gene flow is likely strengthened more by sexual selection than by assortment.

Biased movement drives local cryptic coloration on distinct urban pavements

Explanations of how organisms might adapt to urban environments have mostly focused on divergent natural selection and adaptive plasticity. However, differential habitat choice has been suggested as an alternative. Here, we test for habitat choice in enhancing crypsis in ground-perching grasshoppers colonizing an urbanized environment, composed of a mosaic of four distinctly coloured substrates (asphalt roads and adjacent pavements). Additionally, we determine its relative importance compared to present-day natural selection and phenotypic plasticity. We found that grasshoppers are very mobile, but nevertheless approximately match the colour of their local substrate. By manipulating grasshopper colour, we confirm that grasshoppers increase the usage of those urban substrates that resemble their own colours. This selective movement actively improves crypsis. Colour divergence between grasshoppers on different substrates is not or hardly owing to present-day natural selection, because observed mortality rates are too low to counteract random substrate use. Additional experiments also show negligible contributions from plasticity in colour. Our results confirm that matching habitat choice can be an important driver of adaptation to urban environments. In general, studies should more fully incorporate that individuals are not only selective targets (i.e. selected on by the environment), but also selective agents (i.e. selecting their own environments).

Evidence for mutation-order speciation inSenecio lautus

In a number of animal species, divergent natural selection has repeatedly and independently driven the evolution of reproductive isolation between populations adapted to contrasting, but not to similar environments1. This process is known as parallel ecological speciation, and examples in plants are enigmatically rare2. Here, we perform a comprehensive test of the ecological speciation hypothesis in an Australian wildflower where parapatric populations found in coastal sand dunes (Dune ecotype) and headlands (Headland ecotype) have repeatedly and independently diverged in growth habit. Consistent with a role for divergent natural selection driving the evolution of reproductive isolation, we found that Dune populations with erect growth habit were easy to transplant across sand dunes, were largely interfertile despite half-a-million years of divergence, and were reproductively isolated from equally divergent Headland populations with prostrate growth habit. However, we unexpectedly discovered that both extrinsic and intrinsic reproductive isolation has evolved between prostrate Headland populations, suggesting that populations evolving convergent phenotypes can also rapidly become new species. Mutation-order speciation2, where the random accumulation of adaptive alleles create genetic incompatibilities between populations inhabiting similar habitats, provides a compelling explanation for these complex patterns of reproductive isolation. Our results suggest that natural selection can drive speciation effectively, but environmental and genetic complexity might make parallel ecological speciation uncommon in plants despite strong morphological convergence.

Rapid experimental evolution of reproductive isolation from a single natural population

Ecological speciation occurs when local adaptation generates reproductive isolation as a by-product of natural selection. Although ecological speciation is a fundamental source of diversification, the mechanistic link between natural selection and reproductive isolation remains poorly understood, especially in natural populations. Here, we show that experimental evolution of parasite body size over 4 y (approximately 60 generations) leads to reproductive isolation in natural populations of feather lice on birds. When lice are transferred to pigeons of different sizes, they rapidly evolve differences in body size that are correlated with host size. These differences in size trigger mechanical mating isolation between lice that are locally adapted to the different sized hosts. Size differences among lice also influence the outcome of competition between males for access to females. Thus, body size directly mediates reproductive isolation through its influence on both intersexual compatibility and intrasexual competition. Our results confirm that divergent natural selection acting on a single phenotypic trait can cause reproductive isolation to emerge from a single natural population in real time.

Insights from Fisher’s geometric model on the likelihood of speciation under different histories of environmental change

The formation of new species via the accumulation of incompatible genetic changes is thought to result either from ecologically-based divergent natural selection or the order by which mutations happen to arise, leading to different evolutionary trajectories even under similar selection pressures. There is growing evidence in support of both ecological speciation and mutation-order speciation, but how different environmental scenarios affect the rate of species formation remains underexplored. We use a simple model of optimizing selection on multiple traits (“Fisher’s geometric model”) to determine the conditions that generate genetic incompatibilities in a changing environment. We find that incompatibilities are likely to accumulate in isolated populations adapting to different environments, consistent with ecological speciation. Incompatibilities also arise when isolated populations face a similar novel environment; these cases of mutation-order speciation are particularly likely when the environment changes rapidly and favors the accumulation of large-effect mutations. In addition, we find that homoploid hybrid speciation is likely to occur either when new environments arise in between the parental environments or when parental populations have accumulated large-effect mutations following a period of rapid adaptation. Our results indicate that periods of rapid environmental change are particularly conducive to speciation, especially mutation-order or hybrid speciation.

Parallel genetic evolution and speciation from standing variation

Adaptation often proceeds via the sorting of standing variation, and natural selection acting on pairs of populations is a quantitative continuum ranging from parallel to divergent. Yet, it is unclear how the extent of parallel genetic evolution during adaptation from standing variation is affected by the difference in the direction of selection between populations. Nor is it clear whether the availability of standing variation for adaptation affects progress toward speciation in a manner that depends on the difference in the direction of selection. We conducted a theoretical study investigating these questions and have two primary findings. First, the extent of parallel genetic evolution between two populations is expected to rapidly decline as the difference in their directions of selection increases from fully parallel toward divergent, and this decline occurs more rapidly in organisms with greater trait ‘dimensionality’. This rapid decline results because seemingly small differences in the direction of selection cause steep reductions in the fraction of alleles that are beneficial in both populations. For example, populations adapting to optima separated by an angle of 33° have only 50% of potentially beneficial alleles in common (for a case of five trait ‘dimensions’). Second, we find that adaptation from standing variation leads to higher ecologically-dependent hybrid fitness under parallel selection, relative to when adaptation is from new mutation only. This occurs because genetic parallelism based on standing variation reduces the phenotypic segregation variance in hybrids when parents adapt to similar environments. In contrast, under divergent selection, the pleiotropic effects of alternative alleles fixed from standing variation change the major axes of phenotypic variation in hybrids and reduce their fitness in parental habitats. We conclude that adaptation from standing genetic variation is expected to slow progress toward speciation via parallel natural selection and can facilitate progress toward speciation via divergent natural selection.Impact summaryIt is increasingly clear that much of adaptation, especially that which occurs rapidly, proceeds from the sorting of ancestral standing variation rather than complete reliance on de novo mutation. In addition, evolutionary biologists are increasingly embracing the fact that the difference in the direction of natural selection on pairs of populations is a quantitative continuum ranging from completely parallel to completely divergent. In this article, we ask two questions. First, how does the degree of genetic parallelism—here, adaptation using the same alleles in allopatric populations—depend on the differences in the direction of natural selection acting on two populations, from parallel (0°) to divergent (180°)? And second, how does adaptation from standing variation affect progress toward speciation, and does its effect depend on the direction of natural selection? We develop theory to address these questions. We first find that very small differences in the direction of selection (angle) can largely preclude genetic parallelism. Second, we find that adaptation from standing variation has implications for speciation that change along the continuum from parallel to divergent selection. Under parallel selection, high genetic parallelism causes inter-population hybrids to have high mean fitness when their parents adapt from standing variation. As selection tends toward divergent, adaptation from standing variation is less beneficial for hybrid fitness and under completely divergent selection causes inter-population hybrids to have lower mean fitness than when adaptation was from new mutation alone. In sum, our results provide general insight into patterns of genetic parallelism and speciation along the continuum of parallel to divergent natural selection when adaptation is from standing variation.

Evolution of genetic variance during adaptive radiation

Genetic correlations between traits can bias adaptation away from optimal phenotypes and constrain the rate of evolution. If genetic correlations between traits limit adaptation to contrasting environments, rapid adaptive divergence across a heterogeneous landscape may be difficult. However, if genetic variance can evolve and align with the direction of natural selection, then abundant allelic variation can promote rapid divergence during adaptive radiation. Here, we explored adaptive divergence among ecotypes of an Australian native wildflower by quantifying divergence in multivariate phenotypes of populations that occupy four contrasting environments. We investigated differences in multivariate genetic variance underlying morphological traits and examined the alignment between divergence in phenotype and divergence in genetic variance. We found that divergence in mean multivariate phenotype has occurred along two major axes represented by different combinations of plant architecture and leaf traits. Ecotypes also showed divergence in the level of genetic variance in individual traits, and the multivariate distribution of genetic variance among traits. Divergence in multivariate phenotypic mean aligned with divergence in genetic variance, with most of the divergence in phenotype among ecotypes associated with a change in trait combinations that had substantial levels of genetic variance in each ecotype. Overall, our results suggest that divergent natural selection acting on high levels of standing genetic variation might fuel ecotypic differentiation during the early stages of adaptive radiation.