Genomic consequences of multiple speciation processes in a stick insect

Abstract

Diverse geographical modes and mechanisms of speciation are known, and individual speciation genes have now been identified. Despite this progress, genome-wide outcomes of different evolutionary processes during speciation are less understood. Here, we integrate ecological and spatial information, mating trials, transplantation data and analysis of 86 130 single nucleotide polymorphisms (SNPs) in eight populations (28 pairwise comparisons) of Timema cristinae stick insects to test the effects of different factors on genomic divergence in a system undergoing ecological speciation. We find patterns consistent with effects of numerous factors, including geographical distance, gene flow, divergence in host plant use and climate, and selection against maladaptive hybridization (i.e. reinforcement). For example, the number of highly differentiated ‘outlier loci’, allele-frequency clines and the overall distribution of genomic differentiation were recognizably affected by these factors. Although host use has strong effects on phenotypic divergence and reproductive isolation, its effects on genomic divergence were subtler and other factors had pronounced effects. The results demonstrate how genomic data can provide new insights into speciation and how genomic divergence can be complex, yet predictable. Future work could adopt experimental, mapping and functional approaches to directly test which genetic regions are affected by selection and determine their physical location in the genome.

A Genomic Perspective on the Generation and Maintenance of Genetic Diversity in Herbivorous Insects

“…1B) form host races on two sympatric rosid host species. Pairs of host-associated populations form repeatedly across the landscape, and populations cluster phylogenetically by geography rather than by host plant; this scenario is indicative of repeated parallel divergence (Nosil et al 2012; Soria-Carrasco et al 2014). …”

“…1C; Egan et al 2015), predation in Timema (Fig. 1D; Nosil et al 2012), and host plant nutritional and defensive properties in Acyrthosiphon (Hawthorn and Via 2001). …”

Genome-wide evidence for speciation with gene flow inHeliconiusbutterflies

“…Some loci are likely to be shared between incipient species, while selection maintains divergence at others (Turner et al 2005;Nosil et al 2009). Recently, considerable progress has been made in documenting patterns of genomic divergence between incipient species (Hohenlohe et al 2010;Lawniczak et al 2010;Michel et al 2010;Ellegren et al 2012;Nosil et al 2012;Gagnaire et al 2013). Genome-wide studies of threespine sticklebacks (Hohenlohe et al 2010(Hohenlohe et al , 2012 and Ficedula flycatchers (Ellegren et al 2012) revealed patterns of divergence consistent with a model of ''islands'' of divergence amidst a sea of gene flow.…”

“…This is partly because it is challenging to reconstruct ancestral ranges and therefore almost impossible to know for sure the extent of historical contact between species. Fortunately, genomic approaches are now beginning to allow us to address these long-standing questions from a different angle, by documenting the extent of admixture between species on a genome-wide scale (Kulathinal et al 2009;Ellegren et al 2012;Garrigan et al 2012; The Heliconius Genome Consortium 2012; Nosil et al 2012). Speciation genomics therefore offers an opportunity to address long-standing questions regarding the extent to which divergence and speciation occurs in the face of ongoing gene flow.…”

“…Analyses of genomic divergence therefore need to be complemented with more sensitive tests for gene flow between populations (Kulathinal et al 2009;Ellegren et al 2012;Garrigan et al 2012; The Heliconius Genome Consortium 2012; Nosil et al 2012). A widely used approach is to fit coalescent models (Pinho and Hey 2010), but this can be computationally prohibitive for genomic data sets and requires strong assumptions about population parameters.…”