Abstract
Behavioral barriers to gene flow often evolve faster than intrinsic incompatibilities and can eliminate the opportunity for hybridization between interfertile species. While acoustic signal divergence is a common driver of premating isolation in birds and insects, its contribution to speciation in mammals is less studied. Here we characterize the incidence of, and potential barriers to, hybridization among three closely related species of grasshopper mice (genus Onychomys). All three species use long‐distance acoustic signals to attract and localize mates; Onychomys arenicola and Onychomys torridus are acoustically similar and morphologically cryptic whereas Onychomys leucogaster is larger and acoustically distinct. We used genotyping‐by‐sequencing (GBS) to test for evidence of introgression in 227 mice from allopatric and sympatric localities in the western United States and northern Mexico. We conducted laboratory mating trials for all species pairs to assess reproductive compatibility, and recorded vocalizations from O. arenicola and O. torridus in sympatry and allopatry to test for evidence of acoustic character displacement. Hybridization was rare in nature and, contrary to prior evidence for O. torridus/O. arenicola hybrids, only involved O. leucogaster and O. arenicola. In contrast, laboratory crosses between O. torridus and O. arenicola produced litters whereas O. leucogaster and O. arenicola crosses did not. Call fundamental frequency in O. torridus and O. arenicola was indistinguishable in allopatry but significantly differentiated in sympatry, a pattern consistent with reproductive character displacement. These results suggest that assortative mating based on a long‐distance signal is an important isolating mechanism between O. torridus and O. arenicola and highlight the importance of behavioral barriers in determining the permeability of species boundaries.
Highlights
Understanding the relative contributions of intrinsic and extrinsic mechanisms to repro‐ ductive isolation is a long‐standing challenge in evolutionary biology (Coyne & Orr, 2004; Felsenstein, 1981; Mayr, 1963)
Visual examination of chromatograms from mtDNA sequence revealed “heterozygous” peaks at sites with species‐specific SNPs in 23/49 samples used for allozyme analysis by Sullivan et al (1986), including two samples identified as putative hybrids between O. arenicola and O. torridus (Figure S2)
Our findings suggest that hybridization is extremely rare in Onychomys
Summary
Understanding the relative contributions of intrinsic (genetic, devel‐ opmental) and extrinsic (ecological, behavioral) mechanisms to repro‐ ductive isolation is a long‐standing challenge in evolutionary biology (Coyne & Orr, 2004; Felsenstein, 1981; Mayr, 1963). Recent studies of speciation using ‐generation sequencing indicate substan‐ tial gene flow between closely related taxa despite strong intrinsic and/or extrinsic costs to hybridization (e.g., Cooper, Sedghifar, Nash, Comeault, & Matute, 2018; Rafati et al, 2018; Souissi, Bonhomme, Manchado, Bahri‐Sfar, & Gagnaire, 2018) Such findings emphasize the importance of understanding the behavioral mechanisms under‐ lying assortative mating in determining the permeability of species boundaries upon secondary contact (Kopp et al, 2018). The two smaller spe‐ cies, Onychomys torridus and Onychomys arenicola, are morphologi‐ cally cryptic and were considered a single species until the pair was discriminated by fundamental number of the karyotype (Hinesley, 1979), allozymes (Sullivan et al, 1986), and mitochondrial haplo‐ types (Riddle & Honeycutt, 1990) Both O. torridus and O. arenicola co‐occur with O. leucogaster in arid regions throughout the western United States and northern Mexico but are largely allopatric with re‐ spect to each other (Figure 1a). We conducted mating experiments in the laboratory to determine reproductive compati‐ bility among species
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