Parallel evolution despite low genetic diversity in three-spined sticklebacks.

When populations repeatedly adapt to similar environments they can evolve similar phenotypes based on shared genetic mechanisms (parallel evolution). The likelihood of parallel evolution is affected by demographic history, as it depends on the standing genetic variation of the source population. The three-spined stickleback (Gasterosteus aculeatus) repeatedly colonized and adapted to brackish and freshwater. Most parallel evolution studies in G. aculeatus were conducted at high latitudes, where freshwater populations maintain connectivity to the source marine populations. Here, we analysed southern and northern European marine and freshwater populations to test two hypotheses. First, that southern European freshwater populations (which currently lack connection to marine populations) lost genetic diversity due to bottlenecks and inbreeding compared to their northern counterparts. Second, that the degree of genetic parallelism is higher among northern than southern European freshwater populations, as the latter have been subjected to strong drift due to isolation. The results show that southern populations exhibit lower genetic diversity but a higher degree of genetic parallelism than northern populations. Hence, they confirm the hypothesis that southern populations have lost genetic diversity, but this loss probably happened after they had already adapted to freshwater conditions, explaining the high degree of genetic parallelism in the south.

Temperature change effects on marine fish range shifts: A meta-analysis of ecological and methodological predictors.

The current effects of global warming on marine ecosystems are predicted to increase, with species responding by changing their spatial distributions. Marine ectotherms such as fish experience elevated distribution shifts, as temperature plays a key role in physiological functions and delineating population ranges through thermal constraints. Distributional response predictions necessary for population management have been complicated by high heterogeneity in magnitude and direction of movements, which may be explained by both biological as well as methodological study differences. To date, however, there has been no comprehensive synthesis of the interacting ecological factors influencing fish distributions in response to climate change and the confounding methodological factors that can affect their estimation. In this study we analyzed published studies meeting criteria of reporting range shift responses to global warming in 115 taxa spanning all major oceanic regions, totaling 595 three-dimensional population responses (latitudinal, longitudinal, and depth), with temperature identified as a significant driver. We found that latitudinal shifts were the fastest in non-exploited, tropical populations, and inversely correlated with depth shifts which, in turn, dominated at the trailing edges of population ranges. While poleward responses increased with rate of temperature change and latitude, niche was a key factor in predicting both depth (18% of variation) and latitudinal responses (13%), with methodological predictors explaining between 10% and 28% of the observed variance in marine fish responses to temperature change. Finally, we found strong geographical publication bias and limited taxonomical scope, highlighting the need for more representative and standardized research in order to address heterogeneity in distribution responses and improve predictions in face of changing climate.

Cast away in the Adriatic: Low degree of parallel genetic differentiation in three-spined sticklebacks.

The three-spined stickleback (Gasterosteus aculeatus) has repeatedly and independently adapted to freshwater habitats from standing genetic variation (SGV) following colonization from the sea. However, in the Mediterranean Sea G. aculeatus is believed to have gone extinct, and thus the spread of locally adapted alleles between different freshwater populations via the sea since then has been highly unlikely. This is expected to limit parallel evolution, that is the extent to which phylogenetically related alleles can be shared among independently colonized freshwater populations. Using whole genome and 2b-RAD sequencing data, we compared levels of genetic differentiation and genetic parallelism of 15 Adriatic stickleback populations to 19 Pacific, Atlantic and Caspian populations, where gene flow between freshwater populations across extant marine populations is still possible. Our findings support previous studies suggesting that Adriatic populations are highly differentiated (average FST  ≈ 0.45), of low genetic diversity and connectivity, and likely to stem from multiple independent colonizations during the Pleistocene. Linkage disequilibrium network analyses in combination with linear mixed models nevertheless revealed several parallel marine-freshwater differentiated genomic regions, although still not to the extent observed elsewhere in the world. We hypothesize that current levels of genetic parallelism in the Adriatic lineages are a relic of freshwater adaptation from SGV prior to the extinction of marine sticklebacks in the Mediterranean that has persisted despite substantial genetic drift experienced by the Adriatic stickleback isolates.