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

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.

An efficient pipeline to generate data for studies in plastid population genomics and phylogeography.

PREMISE OF THE STUDY: Seed dispersal contributes to gene flow and is responsible for colonization of new sites and range expansion. Sequencing chloroplast haplotypes offers a way to estimate contributions of seed dispersal to population genetic structure and enables studies of population history. Whole-genome sequencing is expensive, but resources can be conserved by pooling samples. Unfortunately, haplotype associations among single-nucleotide polymorphisms (SNPs) are lost in pooled samples, and treating SNP allele frequencies as independent markers provides biased estimates of genetic structure. METHODS: We developed sampling methodologies and an application, CallHap, that uses a least-squares algorithm to evaluate the fit between observed and predicted SNP allele frequencies from pooled samples based on haplotype network phylogeny structure, thus enabling pooling for chloroplast sequencing for large-scale studies of chloroplast genomic variation. This method was tested using artificially constructed test networks and pools, and pooled samples of Lasthenia californica (California goldfields) from southern Oregon, USA. RESULTS: CallHap reliably recovered network topologies and haplotype frequencies from pooled samples. DISCUSSION: The CallHap pipeline allows for the efficient use of resources for estimation of genetic structure for studies using nonrecombining haplotypes such as intraspecific variation in chloroplast, mitochondrial, bacterial, or viral DNA.