A population genomic analysis of species boundaries: neutral processes, adaptive divergence and introgression between two hybridizing plant species

Abstract

Little is known about the nature of species boundaries between closely related plant species and about the extent of introgression as a consequence of hybridization upon secondary contact. To address these topics we analyzed genome-wide differentiation between two closely related Silene species, Silene latifolia and S. dioica, and assessed the strength of introgression in sympatry. More than 300 AFLP markers were genotyped in three allopatric and three sympatric populations of each species. Outlier analyses were performed separately for sympatric and allopatric populations. Both positive and negative outlier loci were found, indicating that divergent and balancing selection, respectively, have shaped patterns of divergence between the two species. Sympatric populations of the two species were found to be less differentiated genetically than allopatric populations, indicating that hybridization has led to gene introgression. We conclude that differentiation between S. latifolia and S. dioica has been shaped by a combination of introgression and selection. These results challenge the view that species differentiation is a genome-wide phenomenon, and instead support the idea that genomes can be porous and that species differentiation has a genic basis.

Adaptive Variation and Introgression of a CONSTANS-Like Gene in North American Red Oaks

“…FIR013 provides such a marker and our examination of the relative allelic frequencies at the FIR013 locus in parapatric Q. rubra/ Q. ellipsoidalis populations has shown that introgression of the 141 bp allele is consistently higher into the drought tolerant Q. ellipsoidalis than introgression of the 138 bp allele into the mesophilic species, Q. rubra (Table 2, Figure 4; [7]). This pattern of asymmetric introgression of outlier alleles suggests different strength of selection against the 138 bp and 141 bp alleles in non-parental environments if interspecific gene flow is symmetric [41][42][43] as observed in the present study between Q. rubra and Q. ellipsoidalis. In contrast, in the only sympatric population, introgression of the 141 bp into Q. ellipsoidalis is much lower (5%) than introgression of the 138 bp into Q. rubra (19%), suggesting that competition between species might affect introgression at FIR013 outlier alleles.…”

Hybridization in contact zone between temperate European pine species

“…This approach has recently been developed in several model plant species demonstrating the role of hybridization and adaptive introgression in the evolution of irises (Iris; Arnold et al 2004), ecological divergence of sunflowers (Helianthus; Rieseberg et al 2007), and the signatures of divergent and balancing selection in campions (Silene; Minder and Widmer 2008) and poplar (Populus; Lexer et al 2010). So far, a few genes involved in adaptation or speciation have been identified in plants including hybrid sterility loci (Lexer and Widmer 2008), determinants of flower color-linked pollinator shifts (Hoballah et al 2007), and genes involved in hybrid necrosis (Bomblies and Weigel 2007).…”

Nucleotide diversity inSilene latifoliaautosomal and sex-linked genes

“…The data so far collected cannot distinguish whether the difference is due to the predicted reduction in Y N e , or to some process increasing high species-wide diversity for X-linked genes. Possibilities include a higher X than Y mutation rate (although this is the opposite of the expectation for any difference between the mutation rates of the two chromosomes, and the data so far available support that expectation, see Filatov & Charlesworth 2002;Filatov 2005), sexual selection causing a high variance in male reproductive success (Laporte & Charlesworth 2002) or introgression of sequences from another species; hybridization is well known to occur between S. latifolia and S. dioica (Baker 1948;Minder & Widmer 2007) and seems to have led to sequences within each species having recombined into X-linked genes of the other (Atanassov et al 2001;Laporte et al 2005). Population size changes also affect the relative diversity levels of genome regions with different N e (Fay & Wu 1999;Pool & Nielsen 2007).…”