Widespread yet heterogeneous genomic divergence

Abstract

Genetic differentiation during adaptive divergence and speciation is heterogeneous among genomic regions. Some regions can be highly differentiated between populations, for example, because they harbour genes under divergent selection or those causing reproductive isolation and thus are resistant to gene flow. Other regions might be homogenized by gene flow and thus weakly differentiated. Debates persist about the number of differentiated regions expected under divergence with gene flow, and their causes, size, and genomic distribution. In this issue of Molecular Ecology, a study of freshwater stickleback used next-generation sequencing to shed novel insight into these issues (Roesti et al. 2012). Many genomic regions distributed across the genome were strongly differentiated, indicating divergence with gene flow can involve a greater number of loci than often thought. Nonetheless, differentiation of some regions, such as those near the centre of chromosomes where recombination is reduced, was strongly accentuated over others. Thus, divergence was widespread yet highly heterogeneous across the genome. Moreover, different population pairs varied in patterns of differentiation, illustrating how genomic divergence builds up across stages of the speciation process. The study demonstrates how variation in different evolutionary processes, such as selection and recombination rate, can combine to result in similar genomic patterns. Future work could focus on teasing apart the contributions of different processes for causing differentiation, a task facilitated by experimental manipulations.

Response to natural selection in Senecio lautus

“…It is important to note that there are some examples of divergence with gene flow, where regions of the genome have reduced recombination rates due to adaptive genes being trapped in inversions (Noor et al 2001;Rieseberg 2001) or divergent selection reducing the flow of genomic regions containing adaptive genes, relative to neutral regions (Nosil and Feder 2012;Via 2012). However it is generally recognized that gene flow is an antagonistic force in the process of divergence Felsenstein 1981), with the biological species concept defining species based on presence or absence of interbreeding between groups (Mayr 1942).…”

“…This model of speciation is dependent on divergent natural selection between contrasting environments as a primary cause of cessation of gene exchange Nosil 2012), as potentially interbreeding populations are driven toward contrasting adaptive peaks, leading to phenotypic divergence. Reproductive isolation arises when hybrids formed between the divergent populations have intermediate phenotypes and suffer fitness costs as a result, or selection can exclude immigrants based on phenotype environment mismatches.…”

“…Ecological selection arises as individuals interact with their surroundings and can include both biotic and abiotic factors, but the process of ecological speciation requires that selective pressure is divergent, which occurs when there is more than one optimal phenotype, and the selection is driving populations towards these phenotypes in contrasting directions Nosil 2012). Perhaps the best examples of ecological speciation occur when patterns of parallel divergence arise as result of similar adaptations to equivalent selective regimes in multiple geographic locations (Colosimo et al 2005;), a pattern much more likely under divergence based on natural selection rather than random processes.…”

“…Although ecological speciation can occur under any geographic arrangement provided divergent selection is the process driving divergence Nosil 2012), determining the importance of divergent ecological selection and the existence of ecologically dependent reproductive isolation when populations share geographic distributions allows a more targeted analysis of the mechanisms driving differentiation and a more rigorous test of ecological speciation theory.…”

Crossing species boundaries : the hybrid histories of the true geese

“…Studies in speciation and hybridization genomics revealed that levels of genetic differentiation between species can be highly variable across the genome: genetic differentiation accumulates in certain genomic regions, while divergence is hampered in other regions by homogenizing gene flow, resulting in a heterogeneous genomic landscape (Nosil et al, 2009, Nosil and Feder, 2012b, Harrison and Larson, 2016. A consequence of this heterogeneity is that genomes are mosaics of different gene histories (Ellegren et al, 2012, Maddison, 1997, Payseur, 2010) that can be compared to unravel complex speciation and hybridization events (Ottenburghs et al, 2016a, Harrison andLarson, 2014).…”