Multigenerational backcrossing and introgression between two woodrat species at an abrupt ecological transition

Abstract

When organisms experience secondary contact after allopatric divergence, genomic regions can introgress differentially depending on their relationships with adaptation, reproductive isolation, recombination, and drift. Analyses of genome‐wide patterns of divergence and introgression could provide insight into the outcomes of hybridization and the potential relationship between allopatric divergence and reproductive isolation. Here, we generate population genetic data (26,262 SNPs; 353 individuals) using a reduced‐representation sequencing approach to quantify patterns of ancestry, differentiation, and introgression between a pair of ecologically distinct mammals—the desert woodrat (N. lepida) and Bryant's woodrat (N. bryanti)—that hybridize at a sharp ecotone in southern California. Individual ancestry estimates confirmed that hybrids were rare in this bimodal hybrid zone, and entirely consisted of a few F1 individuals and a broad range of multigenerational backcrosses. Genomic cline analyses indicated more than half of loci had elevated introgression from one genomic background into the other. However, introgression was not associated with relative or absolute measures of divergence, and loci with extreme values for both were not typically found near detoxification enzymes previously implicated in dietary specialization for woodrats. The decoupling of differentiation and introgression suggests that processes other than adaptation, such as drift, may underlie the extreme clines at this contact zone.

Weak coupling among barrier loci and waves of neutral and adaptive introgression across an expanding hybrid zone

“…The results of the genomic cline analyses were consistent with the geographic cline analysis in several respects. Compared to previous studies (e.g., Gompert and Buerkle 2012;Gompert et al 2017;Jahner et al 2021;Wen and Fu 2021), the range of the hybrid index was limited (i.e., from ∼0.5 to ∼0.85), which is consistent with a low level of divergence between these two Ranunculus species. Moreover, a high proportion of the clines analyzed displayed excess ancestry, and most of these had centers displaced toward R. austro-oreganus.…”

“… 2017 ; Jahner et al. 2021 ; Wen and Fu 2021 ), the range of the hybrid index was limited (i.e., from ∼0.5 to ∼0.85), which is consistent with a low level of divergence between these two Ranunculus species. Moreover, a high proportion of the clines analyzed displayed excess ancestry, and most of these had centers displaced toward R. austro‐oreganus .…”

Consequences of Hybridization in Mammals: A Systematic Review

“…In woodrat species ( Neotoma bryanti and Neotoma lepida ), a hybrid zone has been maintained as a result of sporadic cross-breeding between these species and hybrid fertility [ 196 ]. Among studies included in this literature review, hybrid zones have been described in mice ( Mus musculus musculus and Mus musculus domesticus ) [ 197 ], different woodrat species [ 195 , 196 , 198 , 199 , 200 ], marmots [ 201 ], primates [ 181 ], artiodactyles [ 157 , 202 ], Diprotodontia [ 203 , 204 ] and carnivores [ 138 , 205 ].…”

The gut microbiome reflects ancestry despite dietary shifts across a hybrid zone

“…Here, Neotoma bryanti (Bryant's woodrat) occurs primarily within the rocky, and relatively mesic, more vegetated, hill habitat (hereafter referred to as "hill") and Neotoma lepida (desert woodrat) occurs primarily within the relatively xeric or arid, Mojave Desert scrub (hereafter referred to as "flats"; Figure 1). Here, the two species hybridise and generate a spectrum of F1 and backcross hybrid genotypes that are distributed within approximately ½ km 2 (Jahner et al, 2021;Patton et al, 2007;Shurtliff et al, 2014). The parental species maintain distinct, habitat-specific and toxic, plantbased diets across the ecotone during both wet and dry seasons (Matocq et al, 2020;Nielsen & Matocq, 2021).…”