Population genomic signatures of divergent adaptation, gene flow and hybrid speciation in the rapid radiation ofLakeVictoria cichlid fishes

Abstract

Adaptive radiations are an important source of biodiversity and are often characterized by many speciation events in very short succession. It has been proposed that the high speciation rates in these radiations may be fuelled by novel genetic combinations produced in episodes of hybridization among the young species. The role of such hybridization events in the evolutionary history of a group can be investigated by comparing the genealogical relationships inferred from different subsets of loci, but such studies have thus far often been hampered by shallow genetic divergences, especially in young adaptive radiations, and the lack of genome-scale molecular data. Here, we use a genome-wide sampling of SNPs identified within restriction site-associated DNA (RAD) tags to investigate the genomic consistency of patterns of shared ancestry and adaptive divergence among five sympatric cichlid species of two genera, Pundamilia and Mbipia, which form part of the massive adaptive radiation of cichlids in the East African Lake Victoria. Species pairs differ along several axes: male nuptial colouration, feeding ecology, depth distribution, as well as the morphological traits that distinguish the two genera and more subtle morphological differences. Using outlier scan approaches, we identify signals of divergent selection between all species pairs with a number of loci showing parallel patterns in replicated contrasts either between genera or between male colour types. We then create SNP subsets that we expect to be characterized to different extents by selection history and neutral processes and describe phylogenetic and population genetic patterns across these subsets. These analyses reveal very different evolutionary histories for different regions of the genome. To explain these results, we propose at least two intergeneric hybridization events (between Mbipia spp. and Pundamilia spp.) in the evolutionary history of these five species that would have lead to the evolution of novel trait combinations and new species.

Outlier analyses to test for local adaptation to breeding grounds in a migratory arctic seabird

“…Akpatok showed the highest number of outliers when compared to Prince Leopold (28 SNPs) and Minarets (24 SNPs), respectively. The 137 SNPs identified among all runs were distributed among 111 loci, and 38 SNPs were indicated as potentially under positive selection in two or more pairwise comparisons, indicating either that populations may be diverging in parallel (Keller et al., 2013) or that these loci are located in area of low recombination (Burri et al., 2015). …”

“…Outlier analyses can be powerful tools to detect loci that are under selection, especially when levels of background genomic differentiation are low (e.g., Hess et al., 2013; Keller et al., 2013; Milano et al., 2014). However, several factors can limit the power of these methods or confound the interpretation of results (Mita et al., 2013; Edwards et al., 2015; Lotterhos & Whitlock, 2014; Narum & Hess, 2011).…”

“…We first investigated genetic differentiation between common and thick‐billed murres to test for hybrids. We then performed clustering analyses to test whether the loci putatively under selection grouped individual thick‐billed murres differently from the complete dataset (as in e.g., Milano et al., 2014; Keller et al., 2013). We analyzed two separate datasets—one that included all loci and one that included only outlier loci—using two different clustering methods.…”

“…An exponential increase in the number of genotyped loci and coverage of the genome over previous methods has also increased power to detect loci that deviate from a neutral model of evolution (i.e., outlier loci) and potentially underlie adaptation. Outlier analyses have allowed researchers to detect loci putatively under selection, which were then able to reveal fine differentiation patterns in otherwise homogenous populations and species (Hess, Campbell, Close, Docker, & Narum, 2013; Keller et al., 2013; Milano et al., 2014). …”

Genomic signatures of population bottleneck and recovery in Northwest Atlantic pinnipeds

“…These studies, using both simulated and empirical data, have quantified the number of retained homologous loci among species with varying divergence dates. Simulations suggest that hundreds of orthologous, phylogenetically informative loci can be identified in species with divergence times of up to 60 million years (Cariou, Duret, & Charlat, 2016a,2016b; Rubin, Ree, & Moreau, 2012), but empirical studies have successfully applied RADseq to phylogenetic studies of species only from more recent radiations (<100,000 years; Keller et al., 2013; Wagner et al., 2013) and find that the number of shared SNPs drops, sometimes quickly, as divergence dates increase (Lexer et al., 2013; Pante et al., 2015). Among our two studied seal species, harbor and gray, that diverged approximately 5 mya (Arnason et al., 2006), we found over 100,000 homologous RAD loci.…”