Species in a common landscape often face similar selective environments. The capacity of organisms to adapt to these environments may be largely species specific. Quantifying shared and unique adaptive responses across species within landscapes may thus improve our understanding of landscape-moderated biodiversity patterns. Here we test to what extent populations of two coexisting and phylogenetically related fishes—three-spined and nine-spined stickleback—differ in the strength and nature of neutral and adaptive divergence along a salinity gradient. Phenotypic differentiation, neutral genetic differentiation and genomic signatures of adaptation are stronger in the three-spined stickleback. Yet, both species show substantial phenotypic parallelism. In contrast, genomic signatures of adaptation involve different genomic regions, and are thus non-parallel. The relative contribution of spatial and environmental drivers of population divergence in each species reflects different strategies for persistence in the same landscape. These results provide insight in the mechanisms underlying variation in evolutionary versatility and ecological success among species within landscapes.

Local adaptation is often obvious when gene flow is impeded, such as observed at large spatial scales and across strong ecological contrasts. However, it becomes less certain at small scales such as between adjacent populations or across weak ecological contrasts, when gene flow is strong. While studies on genomic adaptation tend to focus on the former, less is known about the genomic targets of natural selection in the latter situation. In this study, we investigate genomic adaptation in populations of the three-spined stickleback Gasterosteus aculeatus L. across a small-scale ecological transition with salinities ranging from brackish to fresh. Adaptation to salinity has been repeatedly demonstrated in this species. A genome scan based on 87 microsatellite markers revealed only few signatures of selection, likely owing to the constraints that homogenizing gene flow puts on adaptive divergence. However, the detected loci appear repeatedly as targets of selection in similar studies of genomic adaptation in the three-spined stickleback. We conclude that the signature of genomic selection in the face of strong gene flow is weak, yet detectable. We argue that the range of studies of genomic divergence should be extended to include more systems characterized by limited geographical and ecological isolation, which is often a realistic setting in nature.

Quantifying the contribution of the various processes that influence population genetic structure is important, but difficult. One of the reasons is that no single measure appropriately quantifies all aspects of genetic structure. An increasing number of studies is analyzing population structure using the statistic D, which measures genetic differentiation, next to GST, which is the standardized variance in allele frequencies among populations. Few studies have evaluated which statistic is most appropriate in particular situations. In this study, we evaluated which index is more suitable in quantifying postglacial divergence between three-spined stickleback (Gasterosteus aculeatus) populations from Western Europe. Population structure on this short timescale (10, 000 generations) is likely shaped by colonization history, followed by migration and drift. Using microsatellite markers and anticipating that D and GST might have different capacities to reveal these processes, we evaluated population structure at two levels: 1) between lowland and upland populations, aiming to infer historical processes; and 2) among upland populations, aiming to quantify contemporary processes. In the first case, only D revealed clear clusters of populations, putatively indicative of population ancestry. In the second case, only GST was indicative for the balance between migration and drift. Simulations of colonization and subsequent divergence in a hierarchical stepping stone model confirmed this discrepancy, which becomes particularly strong for markers with moderate to high mutation rates. We conclude that on short timescales, and across strong clines in population size, D is useful to infer colonization history, whereas GST is sensitive for more recent demographic events.

Ecological selection against hybrids between populations occupying different habitats might be an important component of reproductive isolation during the initial stages of speciation. The strength and directionality of this barrier to gene flow depends on the genetic architecture underlying divergence in ecologically relevant phenotypes. We here present line cross analyses of inheritance for two key foraging-related morphological traits involved in adaptive divergence between stickleback ecotypes residing parapatrically in lake and stream habitats within the Misty Lake watershed (Vancouver Island, Canada). One main finding is striking genetic dominance of the lake phenotype for body depth. Selection associated with this phenotype against first and later generation hybrids should therefore be asymmetric, hindering introgression from the lake to the stream population but not vice versa. Another main finding is that divergence in gill raker number is inherited additively and should therefore contribute symmetrically to reproductive isolation. Our study suggests that traits involved in adaptation might contribute to reproductive isolation qualitatively differently, depending on their mode of inheritance.