Abstract
Large chromosomal rearrangements are thought to facilitate adaptation to heterogeneous environments by limiting genomic recombination. Indeed, inversions have been implicated in adaptation along environmental clines and in ecotype specialization. Here, we combine classical ecological studies and population genetics to investigate an inversion polymorphism previously documented in Europe among natural populations of the seaweed fly Coelopa frigida along a latitudinal cline in North America. We test if the inversion is present in North America and polymorphic, assess which environmental conditions modulate the inversion karyotype frequencies, and document the relationship between inversion karyotype and adult size. We sampled nearly 2000 flies from 20 populations along several environmental gradients to quantify associations of inversion frequencies to heterogeneous environmental variables. Genotyping and phenotyping showed a widespread and conserved inversion polymorphism between Europe and America. Variation in inversion frequency was significantly associated with environmental factors, with parallel patterns between continents, indicating that the inversion may play a role in local adaptation. The three karyotypes of the inversion are differently favoured across micro-habitats and represent life-history strategies likely to be maintained by the collective action of several mechanisms of balancing selection. Our study adds to the mounting evidence that inversions are facilitators of adaptation and enhance within-species diversity.
Highlights
Adaptation to heterogeneous environments is a major driver of evolution and in the diversification of life [1,2]
We discuss hereafter how our results allow new insights into this intercontinental inversion polymorphism and how our data suggest a collective role for several mechanisms of balancing selection
In C. frigida, we identified these characteristics in three adjacent coding regions whose haplotypes were perfectly associated with the alcohol dehydrogenase (Adh) allozyme marker of the a/b inversion
Summary
Adaptation to heterogeneous environments is a major driver of evolution and in the diversification of life [1,2]. Each population may follow its own evolutionary trajectory driven by local environmental conditions [1,3] This can result in genetic and phenotypic polymorphism, variation at adaptive traits between habitats or along environmental clines, and, diversification into ecotypes or species [3 –5]. Polymorphisms may be maintained by gene flow or if balancing selection is involved [25,26,27,28,29] To disentangle these mechanisms, it is useful to combine knowledge of inversion effects on phenotypes with ecological and molecular data on natural populations harbouring the inversion across environmental gradients. The sampled area follows a latitudinal cline, a gradient of salinity into the St Lawrence Estuary, and spans a heterogeneous seaweed distribution This allowed investigating separately the effects of different environmental parameters on the inversion frequency and testing the extent of parallelism with Europe. We set out to determine if the inversion is present in North America and polymorphic, which environmental conditions modulate the inversion karyotype frequencies, and the relationship between inversion karyotype and adult size
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