Demography and Selection Shape Transcriptomic Divergence in Field Crickets

ABSTRACTGene flow, demography, and selection can result in similar patterns of genomic variation and disentangling their effects is key to understanding speciation. Here, we assess transcriptomic variation to unravel the evolutionary history of Gryllus rubens and Gryllus texensis, cryptic field cricket species with highly divergent mating behavior. We infer their demographic history and screen their transcriptomes for footprints of selection in the context of the inferred demography. We find strong support for a long history of bidirectional gene flow, which ceased during the late Pleistocene, and a bottleneck in G. rubens consistent with a peripatric origin of this species. Importantly, the demographic history has likely strongly shaped patterns of neutral genetic differentiation (empirical FST distribution). Concordantly, FST based selection detection uncovers a large number of outliers, likely comprising many false positives, echoing recent theoretical insights. Alternative genetic signatures of positive selection, informed by the demographic history of the sibling species, highlighted a smaller set of loci; many of these are candidates for controlling variation in mating behavior. Our results underscore the importance of demography in shaping overall patterns of genetic divergence and highlight that examining both demography and selection facilitates a more complete understanding of genetic divergence during speciation.

Molecular divergence between Gryllus rubens and Gryllus texensis, sister species of field crickets (Orthoptera: Gryllidae)

We assess the degree of sequence divergence in the maternally inherited mitochondrial cytochrome c oxidase I (COI) and cytochrome b (CytB) genes between two sister species of field crickets, Gryllus rubens Scudder, 1902 and Gryllus texensis Cade and Otte, 2000. We analyzed 1460 base pairs from 10 individuals of each species; individuals were sampled from areas of both allopatry and sympatry. Overall average pairwise mitochondrial sequence divergence between species was 1.4% ± 0.1% (mean ± SD); however, there was almost an order of magnitude more divergence in COI (2.59% ± 2.25%) than in CytB (0.35% ± 0.24%). Gryllus texensis appears to harbor a much greater level of genetic variation than does G. rubens. Phylogenetic trees constructed from these sequences show reasonable separation of species; however, sequences are not reciprocally monophyletic. Gene tree polyphyly may reflect recent species-level divergence and (or) interspecific gene flow. The pattern of sequence divergence and genetic variation in these taxa is consistent with allopatric or peripatric speciation in Pleistocene glacial refugia in the southeastern (G. rubens ancestral lineage) and southcentral United States (G. texensis ancestral lineage).