Levels of genetic differentiation can be highly variable across the genome, a pattern we refer to here as ‘heterogeneous genomic divergence’ (Harrison 1991; Avise 2000; Rieseberg 2001; Via 2001; Wu 2001; Ortiz-Barrientos et al. 2002; Orr et al. 2004; Wu & Ting 2004; Gavrilets & Vose 2005; Mallet 2005; Turner et al. 2005; Harr 2006; Noor & Feder 2006; Begun et al. 2007; Mallet et al. 2007; Via & West 2008; see glossary for terminology). Genomic divergence may be particularly heterogeneous during the process of population divergence and speciation, during which genetic differentiation accumulates in some regions, while the homogenizing effects of gene flow or inadequate time for random differentiation by genetic drift precludes divergence in other regions (Wu 2001; Gavrilets & Vose 2005). Many factors potentially contribute to heterogeneous genomic divergence, including selection arising from ecological causes (Schluter 2000; Wu 2001) or genetic conflict (Rice 1998; Presgraves et al. 2003; Haig 2004; Arnqvist & Rowe 2005; Crespi 2007; Presgraves 2007), the stochastic effects of genetic drift (Kimura 1968, 1986; King & Jukes 1969; Ohta 1992, 2002), variable mutation rates (Balloux & Lugon-Moulin 2002; Hedrick 2005; Noor & Feder 2006), the genomic distribution and effect size of genes under selection (Orr 2005), and chromosomal structure (Noor et al. 2001; Rieseberg 2001; Ortiz-Barrientos et al. 2002).
We focus here on the contributions of divergent selection, defined as selection that acts in contrasting directions in two populations (cf. Schluter 2000; Rundle & Nosil 2005). Divergent selection itself can promote molecular genetic differentiation via two main mechanisms: (i) by acting on specific loci and those physically linked to them (Fisher 1930; Haldane 1930, 1932; Endler 1973; Lewontin & Krakauer 1973; Barton 2000), and (ii) by promoting reproductive isolation that causes barriers to gene flow (i.e. ‘ecological speciation’, Mayr 1963; Funk 1998; Schluter 2000; Rundle & Nosil 2005), thereby facilitating even genome-wide neutral divergence via genetic drift. The first mechanism involves a relatively direct role for selection in genetic differentiation and promotes divergence both in the presence and absence of gene flow (Fig. 1). The second mechanism facilitates differentiation by a different process (drift). This second mechanism applies only to divergence with gene flow because in allopatric scenarios, divergent selection is not required to counter gene flow in order for neutral population differentiation to proceed. While these basic mechanisms account for heterogeneity in the origin and frequency of highly differentiated genomic regions, and in their degree of differentiation, selection may also affect the actual size of such ‘islands of genomic divergence’ on a chromosome (Turner et al. 2005; Harr 2006; Begun et al. 2007; Turner & Hahn 2007; see glossary).
Here, we review these roles for divergent selection in generating heterogeneous genomic divergence, and further consider the nature and growth of islands of genomic divergence. We consider mainly conceptual issues and empirical patterns, because methodology has been well covered elsewhere (e.g. Beaumont & Nichols 1996; Andolfatto 2001; Black et al. 2001; Schlötterer 2002; Luikart et al. 2003; Beaumont & Balding 2004; Beaumont 2005; Nielsen 2005; Storz 2005; Vasemagi & Primmer 2005; Hahn 2006; Hedrick 2006; Noor & Feder 2006; Bonin et al. 2007; Foll & Gaggiotti 2008; Riebler et al. 2008; Stinchcombe & Hoekstra 2008). We focus on divergence during the process of population differentiation and speciation, and note that during this process, loci under divergent selection and loci causing reproductive isolation behave similarly, differentiating more strongly (even during allopatric divergence), and introgressing less freely than other loci (Barton 1979, 1983; Barton & Hewitt 1989; Mallet 1995, 2005, 2006; Wu 2001; Wu & Ting 2004; Nosil et al. 2005). While acknowledging this similarity (see the Supporting information for further discussion), we focus on divergent selection per se. Our frequent use of ‘selection’ is shorthand for ‘divergent selection’, while ‘genetic differentiation’ refers to ‘molecular genetic differentiation’.
In the order presented, the specific aims of this study are to: (i) discuss theory and make explicit predictions about divergent selection and heterogeneous genomic divergence (Table 1), aided by the metaphor of genomic islands of divergence, (ii) review empirical studies testing for loci whose genetic divergence exceed neutral expectations, that is, ‘outlier loci’, which putatively represent the genetic signature of divergent selection, (iii) review empirical studies testing whether adaptive phenotypic divergence facilitates molecular genetic differentiation, (iv) describe how selection may promote the growth of genomic islands of divergence, and (v) integrate our findings and offer suggestions for future research.
|Type of locus||Predictions|
|Locus directly under selection||— strong genetic divergence at these loci (as illustrated by, e.g. outlier status)|
|Locus tightly physically linked to those under selection||— strong genetic divergence at these loci (as illustrated by, e.g. outlier status)|
|Locus loosely physically linked to those under selection||— moderately increased genetic divergence compared to neutrality|
|— IBA pattern should be observed even beyond the spatial scale of gene flow (e.g. among completely allopatric populations)|
|Neutral, unlinked loci (affected by ‘general barriers’)||— IBA expected at the spatial scale of gene flow if gene flow is sufficiently reduced to allow divergence via genetic drift (i.e. selection and reproductive isolation must be strong);|
|— likelihood of IBA increases with decreasing Ne (i.e. as drift becomes more effective)|
|Models for growth of differentiated regions||Predictions|
|I. Allopatric model||— many differentiated regions (i.e. ‘genomic islands’)|
|— islands need not be clustered within the genome, and will often be small in size|
|— number and elevation of islands increases with time since population divergence|
|II. Ecological model (divergent selection with gene flow)||— large islands will occur|
|— genomic clustering of islands, with genes affecting local adaptation and reproductive isolation residing within these clusters, perhaps fewer islands than the allopatric model|
|— islands need not involve chromosomal inversions (e.g. supergenes)|
|— small islands, which have not yet grown, are also possible|
|III. Structural model||— genomic differentiation is facilitated by chromosomal inversions and other factors that reduce recombination, dependent on the degree to which genes affecting local adaptation and reproductive isolation reside within inversions|
|— the extent of this facilitation also depends on how far outside an inversion the introgression reducing effects of the inversion extend|
|— islands can be larger than in the other models, and persist for longer periods of time|