Importance of incomplete lineage sorting and introgression in the origin of shared genetic variation between two closely related pines with overlapping distributions

Abstract

Genetic variation shared between closely related species may be due to retention of ancestral polymorphisms because of incomplete lineage sorting (ILS) and/or introgression following secondary contact. It is challenging to distinguish ILS and introgression because they generate similar patterns of shared genetic diversity, but this is nonetheless essential for inferring accurately the history of species with overlapping distributions. To address this issue, we sequenced 33 independent intron loci across the genome of two closely related pine species (Pinus massoniana Lamb. and Pinus hwangshanensis Hisa) from Southeast China. Population structure analyses revealed that the species showed slightly more admixture in parapatric populations than in allopatric populations. Levels of interspecific differentiation were lower in parapatry than in allopatry. Approximate Bayesian computation suggested that the most likely speciation scenario explaining this pattern was a long period of isolation followed by a secondary contact. Ecological niche modeling suggested that a gradual range expansion of P. hwangshanensis during the Pleistocene climatic oscillations could have been the cause of the overlap. Our study therefore suggests that secondary introgression, rather than ILS, explains most of the shared nuclear genomic variation between these two species and demonstrates the complementarity of population genetics and ecological niche modeling in understanding gene flow history. Finally, we discuss the importance of contrasting results from markers with different dynamics of migration, namely nuclear, chloroplast and mitochondrial DNA.

Genetic evidence for species cohesion, substructure and hybrids in spruce

“…Problems arise when isolated lineages emerge in rapid succession (adaptive radiation) or when previously isolated groups exchange allelic variation through gene flow (hybridization and introgression). The relative ease with which informative genetic polymorphisms can now be obtained through DNA sequencing means that some previously intractable relationships between groups can be reconstructed (e.g., Lamichhaney et al, ; Martin et al, ; McVay et al, ; Meier et al, ; Wagner et al, ) and that sampling of taxa and populations can more comprehensively assay genetic variation near the species level and tie it to evolutionary processes (e.g., Gompert et al, ; Mandeville, Parchman, McDonald, & Buerkle, ; Parchman, Buerkle, Soria‐Carrasco, & Benkman, ; Zhou et al, ). The advances in sequencing are particularly important to improving our understanding of the evolutionary context of trait variation when taxa are only slightly genetically differentiated and when they have large geographical ranges that can accommodate substantial isolation by distance.…”

“…For example, many studies have evaluated local adaptation and the fit of plant phenotypes and genotypes to contemporary environments and climate variation, and have done so within an implicit or explicit framework for the relevant evolutionary history, including species boundaries, hybridization and gene flow (Alberto et al, 2013;Lind et al, 2017;Lindtke, Gompert, Lexer, & Buerkle, 2014;Yeaman et al, 2016). The evolutionary and historical context for studies of trait variation will determine what processes and dy- obtained through DNA sequencing means that some previously intractable relationships between groups can be reconstructed (e.g., Lamichhaney et al, 2015;Martin et al, 2015;McVay et al, 2017;Meier et al, 2017;Wagner et al, 2013) and that sampling of taxa and populations can more comprehensively assay genetic variation near the species level and tie it to evolutionary processes (e.g., Gompert et al, 2014;Mandeville, Parchman, McDonald, & Buerkle, 2015;Parchman, Buerkle, Soria-Carrasco, & Benkman, 2016;Zhou et al, 2017). The advances in sequencing are particularly important to improving our understanding of the evolutionary context of trait variation when taxa are only slightly genetically differentiated and when they have large geographical ranges that can accommodate substantial isolation by distance.…”

Combining mitochondrial and nuclear genome analyses to dissect the effects of colonization, environment, and geography on population structure in Pinus tabuliformis

“…The high diversity and large effective population sizes of P. tabuliformis could be also contributed by introgression from relatives currently or previously parapatric with P. tabuliformis . Interspecific hybridization has been well documented in Asian Pinus species (e.g., Wang et al., ; Yang et al., ; Zhou et al., ) and shared mito‐ and chlorotypes are commonly found in zones of contact or via long‐distance dispersal (Wang et al., ; Yang et al., ). A genomewide scan together with sampling of all neighboring sister species would be required to assess the impact of introgression on genome diversity in P. tabuliformis .…”

Testing reticulate evolution of fourVitisspecies from East Asia using restriction‐site associated DNA sequencing

“…2), which might be attributable to recent introgression events and/or incomplete lineage sorting. Introgression is expected to occur more frequently in sympatric populations or among parapatric populations than among distantly located populations; in contrast, incomplete lineage sorting is expected to result in evenly shared ancestral polymorphism in all populations (Muir & Schl€ otterer, 2005;Zhou et al, 2017). In order to explore whether the genetic variation shared among V. romanetii, V. shenxiensis, and V. piasezkii is caused by introgression or not, we compared patterns of genetic diversity between sympatric populations and allopatric populations of these three species.…”