Asymmetry matters: A genomic assessment of directional biases in gene flow between hybridizing spruces.

Abstract

Assessing directional bias in interspecific gene flow might be important in determining the evolutionary trajectory of closely related species pairs. Using a set of 300 single nucleotide polymorphisms (SNPs) having variable propensity to cross species boundary, we evaluated the genomic extent and direction of interspecific gene flow in a progenitor‐derivative spruce species pair (black spruce and red spruce). A higher rate of gene flow was found from black spruce toward red spruce purebreds than vice versa. This asymmetry could reflect the historical gene flow between the two taxa at the time of species inception and during postglacial colonization. A clear asymmetry in introgression was depicted by a greater gene flow between red spruce and hybrids than between black spruce and hybrids. While backcrossing toward red spruce was invariably high across the genome, the actual species boundary is between hybrids and black spruce where gene flow is impeded at those genomic regions impermeable to introgression. Associations between hybrid index and climatic variables (total annual precipitation and mean annual temperature) were tested, as these might indicate a role for exogenous selection in maintaining the species boundary. While an apparent association was found between the hybrid index and precipitation, it collapsed when considered in light of the directional bias in interspecific gene flow. Hence, considering asymmetrical patterns of introgression allowed us to falsify an apparent role for exogenous selection. Although this was not formerly tested here, we suggest that this pattern could result from asymmetrical endogenous selection, a contention that deserves further investigations.