Quantitative genetic inheritance of morphological divergence in a lake-stream stickleback ecotype pair: implications for reproductive isolation

Abstract

Ecological selection against hybrids between populations occupying different habitats might be an important component of reproductive isolation during the initial stages of speciation. The strength and directionality of this barrier to gene flow depends on the genetic architecture underlying divergence in ecologically relevant phenotypes. We here present line cross analyses of inheritance for two key foraging-related morphological traits involved in adaptive divergence between stickleback ecotypes residing parapatrically in lake and stream habitats within the Misty Lake watershed (Vancouver Island, Canada). One main finding is the striking genetic dominance of the lake phenotype for body depth. Selection associated with this phenotype against first-and later-generation hybrids should therefore be asymmetric, hindering introgression from the lake to the stream population but not vice versa. Another main finding is that divergence in gill raker number is inherited additively and should therefore contribute symmetrically to reproductive isolation. Our study suggests that traits involved in adaptation might contribute to reproductive isolation qualitatively differently, depending on their mode of inheritance

Modularity: Genes, Development, and Evolution

“…Since local variation is not preserved, it is hard to detect local associations and covariation in populations using GPA, limiting its use for the study of modularity. This is also a problem when relating genetic variation to morphological variation, since again variation will be spread out over the whole morphological structure, and local genetic factors will appear to have widespread effect (Berner et al 2011). There have been promising efforts to reconcile landmark based methods and local variation, such as the local shape variables described in Márquez et al (2012), finite element scaling analysis (FESA, Cheverud & Richtsmeier 1986), and euclidean distance matrix analysis (EDMA, Lele & Richtsmeier 1991), but these have not yet been widely adopted.…”

Key questions in the genetics and genomics of eco-evolutionary dynamics

“…Interestingly, dominance appears important between host races of phytophagous insects in general, particularly with respect to performance on the different hosts (Matsubayashi et al, 2010). Mixtures of additive and non-additive effects on adaptive divergence also have been described for many other groups, such as lake versus stream threespine stickleback (Berner et al, 2011) and dwarf versus normal lake whitefish (Coregonus clupeaformis) (Renaut et al, 2009;Bernatchez et al, 2010). Beyond these specific examples, the potential generality of non-additive effects was considered by Roff and Emerson (2006) in their meta-analysis of line cross analyses.…”

Lake-Stream Divergence in Stickleback Life History: A Plastic Response to Trophic Niche Differentiation?

“…In all these scenarios involving phenotypic plasticity, reproductive barriers will arise within a single generation and set the stage for further divergence through allele frequency changes. Despite this potentially important role of plasticity in speciation, however, research efforts are generally directed to deciphering how genetically based trait differences between diverging populations contribute to reproductive isolation (e.g., Hatfield 1997;Hawthorne and Via 2001;Lexer et al 2004;Rogers and Bernatchez 2006;Terai et al 2006;Rego et al 2007;Fuller 2008;Kitano et al 2009;Lowry and Willis 2010;Berner et al 2011;Streisfeld et al 2013;Arnegard et al 2014;Chung et al 2014; but see Payne et al 2000;Kozak et al 2011;Smith et al 2013). …”