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

Abstract

Hybridization can serve as an evolutionary stimulus, but we have little understanding of introgression at early stages of hybrid zone formation. We analyze reproductive isolation and introgression between a range-limited and a widespread species. Reproductive barriers are estimated based on differences in flowering time, ecogeographic distributions, and seed set from crosses. We find an asymmetrical mating barrier due to cytonuclear incompatibility that is consistent with observed clusters of coincident and concordant tension zone clines (barrier loci) for mtDNA haplotypes and nuclear SNPs. These groups of concordant clines are spread across the hybrid zone, resulting in weak coupling among barrier loci and extensive introgression. Neutral clines had nearly equal introgression into both species' ranges, whereas putative cases of adaptive introgression had exceptionally wide clines with centers shifted toward one species. Analyses of cline shape indicate that secondary contact was initiated within the last 800 generations with the per-generation dispersal between 200 and 400 m, and provide some of the first estimates of the strength of selection required to account for observed levels of adaptive introgression. The weak species boundary between these species appears to be in early stages of dissolution, and ultimately will precipitate genetic swamping of the range-limited species.

Testing Wright’s Intermediate Population Size Hypothesis – When Genetic Drift is a Good Thing

“…In one case, there was rapid evolution of antibiotic resistance in Pseudomonas aeruginosa even when population bottlenecks were severe and selection was weak (Mahrt et al 2021). Rapid acquisition of adaptive genetic variants also seems to have occurred in a case of recent budding speciation (peripatric speciation; Mayr 1954) in a range-restricted species of buttercup (Cruzan et al 2021). In all of these cases, adaptation to novel conditions appears to have occurred quickly during periods of reduced population size and suggests drift facilitation of selection may be a widespread phenomenon.…”

“…Moreover, reductions in population size due to bottlenecks and founder events are likely to be associated with increased environmental stress, and consequently we expect selection to often increase during population bottlenecks (Fowler and Whitlock 2002; Matute 2013). Higher frequencies of segregating mutations along with drift facilitation may be responsible for elevated levels of purging following population bottlenecks (Bouzat 2010), and may help explain the substantial number of cases of rapid adaption during episodes of reduced population size (e.g., Carvalho et al 1996; Rosenblum et al 2007; Tepolt et al 2009; Marsico et al 2011; Cruzan 2019; Rego et al 2019; Cruzan et al 2021; Mahrt et al 2021; Yin et al 2021; van der Zee et al 2022). On the other hand, we expect population bottlenecks and founder events to result in elevated accumulation of drift load (Lynch et al 1995; Willi et al 2013), but the simulations presented here indicate the potential for purging segregation load and the fixation of deleterious mutations depends on the severity of the reduction in population size.…”

“…Verne Grant (1963, 1981) expanded on the idea of quantum evolution to include rapid speciation events in small, isolated populations at the periphery of a widespread species’ range (budding or peripatric speciation; Mayr 1954). While interest in the idea of quantum evolution has waned, evidence of rapid evolution associated with population bottlenecks continues to accumulate (e.g., Carvalho et al 1996; Rosenblum et al 2007; Tepolt et al 2009; Marsico et al 2011; Cruzan 2019; Rego et al 2019; Cruzan et al 2021; Mahrt et al 2021; Yin et al 2021; van der Zee et al 2022). Surprisingly, there have been no attempts to assess the potential for drift facilitation of selection in populations of intermediate size using analytical or numerical approaches.…”

Effects of the neo‐X chromosome on genomic signatures of hybridization inRumex hastatulus

“…However, allele frequency clines are often heterogeneous across the genome of hybrid individuals (Aeschbacher et al, 2017; Brandvain et al, 2014; Gibson and Moyle, 2019; Rieseberg et al, 1995; Rifkin et al, 2019). Genomic regions resistant to the shuffling of alleles can maintain reproductive incompatibilities between species, and loci at which the allele frequency cline is steep can be an indication of linkage with such incompatibilities (Barton 1983; Barton and Bengtsson, 1986; Cruzan et al, 2021; Gompert et al, 2017). Hybrid zones can therefore provide opportunities for insights into the genetic mechanisms governing reproductive isolation in natural populations.…”

Genomic signatures of hybridization on the neo-X chromosome ofRumex hastatulus

“…However, allele frequency clines are often heterogeneous across the genome of hybrid individuals (Aeschbacher et al 2017; Brandvain et al 2014; Gibson and Moyle 2019; Rieseberg et al 1995; Rifkin et al 2019). Genomic regions resistant to the shuffling of alleles can maintain reproductive incompatibilities between species, and loci at which the allele frequency cline is steep can be an indication of genes involved with such incompatibilities (Barton 1983; Barton and Bengtsson 1986; Cruzan et al 2021; Gompert et al 2017). Hybrid zones can therefore provide opportunities for direct insights into the genetic mechanisms governing reproductive isolation in natural populations.…”