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Changes in selection pressure can facilitate hybridization during biological invasion in a Cuban lizard

Citation

Bock, Dan et al. (2021), Changes in selection pressure can facilitate hybridization during biological invasion in a Cuban lizard, Dryad, Dataset, https://doi.org/10.5061/dryad.hdr7sqvjg

Abstract

Hybridization is among the evolutionary mechanisms most frequently hypothesized to drive the success of invasive species, in part because hybrids are common in invasive populations. One explanation for this pattern is that biological invasions coincide with a change in selection pressures that limit hybridization in the native range. To investigate this possibility, we studied the introduction of the brown anole (Anolis sagrei) in the southeastern United States. We find that native populations are highly genetically structured. In contrast, all invasive populations show evidence of hybridization among native-range lineages. Temporal sampling in the invasive range spanning 15 years showed that invasive genetic structure has stabilized, indicating that large-scale contemporary gene flow is limited among invasive populations and that hybrid ancestry is maintained. Additionally, our results are consistent with hybrid persistence in invasive populations resulting from changes in natural selection that occurred during invasion. Specifically, we identify a large-effect X chromosome locus associated with variation in limb length, a well-known adaptive trait in anoles, and show that this locus is often under selection in the native range, but rarely so in the invasive range. Moreover, we find that the effect size of alleles at this locus on limb length is much reduced in hybrids among divergent lineages, consistent with epistatic interactions. Thus, in the native range, epistasis manifested in hybrids can strengthen extrinsic post-mating isolation. Together, our findings show how a change in natural selection can contribute to an increase in hybridization in invasive populations.

Methods

These data were obtained from multiple populations across the range of A. sagrei (including Cuba, Bahamas, Florida and Southern Georgia), and consist of genomic and morphological data. The genomic data were obtained using double-digest RAD-seq. The VCF files included in this archive have been filtered using methods described in Bock et al. (2021). The scripts needed to perform these filtering steps are also included in the data archive. The raw reads used at the beginning of the analyses have been deposited on the NCBI SRA (accession numbers are given in Dataset S1 of Bock et al. 2021). The morphological data (also included in Dataset S2 of Bock et al. 2021) were obtained from X-ray images. The specimens used to collect these morphological data along with associated X-ray images have been deposited in the Herpetological Collection of the Harvard Museum of Comparative Zoology (MCZ; museum identification codes are given in Dataset S1 of Bock et al. 2021). Backup tail tip tissue for these specimens is maintained in the cryogenic collection at MCZ.

Funding

Natural Sciences and Engineering Research Council of Canada, Award: 502659

Natural Sciences and Engineering Research Council of Canada, Award: 411730

National Science Foundation, Award: IOS-1827647

National Science Foundation, Award: DEB-1354897

John Templeton Foundation, Award: 52287

National Science Foundation, Award: DEB-1927194