Selection and Dispersal in a Multispecies Oak Hybrid Zone

Abstract

The four western North American red oak species (Quercus wislizeni, Q. parvula, Q. agrifolia, and Q. kelloggii) are known to produce hybrid products in all interspecific combinations. However, it is unknown whether hybrids are transitory resulting from interspecific gene flow or whether they are maintained through extrinsic selection. Here, we examine cryptic hybrid structure in Q. wislizeni through a broad region including contact and isolation from three other western North American red oaks using amplified fragment length polymorphism molecular markers. All four species were simultaneously detected in the genetic background of individuals morphologically assigned to Q. wislizeni, although the contribution of Q. kelloggii was minor. In some cases, introgression was detected well outside the region of sympatry with one of the parental species. Molecular structure at the individual level indicated this was due to long-distance pollen dispersal and not to local extinction of parental species. Species admixture proportions were correlated with climatic variables and greater proportions of Q. agrifolia and Q. parvula were present in the genetic background of Q. wislizeni in sites with cooler and more humid summers, corresponding with habitat preferences of the parental species. Partial Mantel tests indicated that climate was more important than distance from pollen source in this association. Despite high levels of introgression, species integrity was maintained in some populations in close proximity to the other species, providing further support to environmental selection in determining population genetic structure. Thus, the contribution of species mixtures to population genetic structure varies across the landscape according to availability of pollen, but more importantly to varying environmental selection pressures that produce a complex pattern of hybrid and pure gene pools.

Interspecific gene flow and maintenance of species integrity in oaks

“…Likewise, the distribution of Q. robur and Q. petraea in adult sympatric stands is strongly correlated with different ecological requirements with regard to water availability (Cochard et al 1992, Breda et al 1993, and in a mixed Q. petraea / Q. pyrenaica stand in Central Spain hybrids were located in "areas of maximum contact" between both parental species in different micro-environments (de Heredia et al 2009). In the western North American red oak species Q. wislizeni, Q. parvula, Q. agrifolia and Q. kelloggii, proportions of hybrids and introgressive forms were more strongly correlated with climate variables than with distance also suggesting ecologically-driven selection (Dodd & Afzal-Rafi i 2004).…”

A nuclear DNA barcode for eastern North American oaks and application to a study of hybridization in an Arboretum setting

“…Hybridization in the genus is common and known to be dependent on spatial distribution of parent trees, pollen dispersal and pollination time, and sexual barriers among other factors (Lagache, Klein, Guichoux, & Petit, 2013; Petit, Bodénès, Ducousso, Roussel, & Kremer, 2004). Oak species with similar reproductive strategies and overlapping geographic regions often hybridize in natural stands (Chybicki & Burczyk, 2010; Curtu, Gailing, & Finkeldey, 2007; Dodd & Afzal‐Rafii, 2004; Dumolin‐Lapègue, Démesure, Fineschi, Le Corre, & Petit, 1997; Dumolin‐Lapègue, Kremer, & Petit, 1999; Efrain Tovar‐Sanchez, 2004; Gerber et al., 2014; Hipp & Weber, 2008; Lexer, Kremer, & Petit, 2006; Moran, Willis, & Clark, 2012; Petit, 1993; Petit et al., 2004; Whittemore & Schaal, 1991). Morphological intermediacy, however, is an imperfect predictor of genetic admixture in oaks, making hybrids difficult to identify (Burgarella et al., 2009; Song, Deng, Hipp, & Li, 2015; Wei, Li, Zhang, & Liao, 2015).…”

“…Morphological intermediacy, however, is an imperfect predictor of genetic admixture in oaks, making hybrids difficult to identify (Burgarella et al., 2009; Song, Deng, Hipp, & Li, 2015; Wei, Li, Zhang, & Liao, 2015). Moreover, multispecies hybrid zones are common in oaks and particularly difficult to study due to sampling issues and selection of adequate numbers of informative loci (Craft & Ashley, 2006; Dodd & Afzal‐Rafii, 2004; Peñaloza‐Ramírez et al., 2010; Sullivan, Owusu, Weber, Hipp, & Gailing, 2016). …”

Hybridization and divergence in multi-species oak (Quercus) communities

“…Conversely, hybridization can erode species coherence and lead to the homogenization of previously distinct gene pools (Seehausen, 2006;Vonlanthen et al, 2012). However, recurrent hybridization among oaks has apparently not led to a loss of genetic or adaptive distinctiveness (Whittemore & Schaal, 1991;Dodd & Afzal-Rafii, 2004;Petit et al, 2004;Curtu, Gailing & Finkeldey, 2007;Peñaloza-Ram ırez et al, 2010). Oaks thus present an opportunity to study how species coherence can be maintained with ongoing gene flow (Arnold & Bennett, 1993;Dodd & Afzal-Rafii, 2004), despite the fact that hybridization has been shown to counteract species divergence in other taxa (Seehausen, 2006;Vonlanthen et al, 2012).…”