Genome‐wide patterns of standing genetic variation in a marine population of three‐spined sticklebacks

Abstract

Since the end of the Pleistocene, the three-spined stickleback (Gasterosteus aculeatus) has repeatedly colonized and adapted to various freshwater habitats probably originating from ancestral marine populations. Standing genetic variation and the underlying genomic architecture both have been speculated to contribute to recent adaptive radiations of sticklebacks. Here, we expand on the current genomic resources of this fish by providing extensive genome-wide variation data from six individuals from a marine (North Sea) stickleback population. Using next-generation sequencing and a combination of paired-end and mate-pair libraries, we detected a wide size range of genetic variation. Among the six individuals, we found more than 7% of the genome is polymorphic, consisting of 2599111 SNPs, 233464 indels and structural variation (SV) (>50 bp) such as 1054 copy-number variable regions (deletions and duplications) and 48 inversions. Many of these polymorphisms affect gene and coding sequences. Based on SNP diversity, we determined outlier regions concordant with signatures expected under adaptive evolution. As some of these outliers overlap with pronounced regions of copy-number variation, we propose the consideration of such SV when analysing SNP data from re-sequencing approaches. We further discuss the value of this resource on genome-wide variation for further investigation upon the relative contribution of standing variation on the parallel evolution of sticklebacks and the importance of the genomic architecture in adaptive radiation.

Parallel evolution and adaptation to environmental factors in a marine flatfish: Implications for fisheries and aquaculture management of the turbot (Scophthalmus maximus)

“…Although still a controversial topic, balancing selection (or parallel evolution) has been identified as an important factor in the evolution of some marine species, for example, related to coral reef fishes (Gaither et al., 2015), European sea bass (Lemaire et al., 2000), and three‐spined stickleback (Feulner et al., 2013; Guo, DeFaveri, Sotelo, Nair, & Merilä, 2015). Moreover, it has also been suggested to play an important role in invasive processes of aquatic organisms (Vera, Díez‐del‐Molino, & García‐Marín, 2016b).…”

“…Moreover, it has also been suggested to play an important role in invasive processes of aquatic organisms (Vera, Díez‐del‐Molino, & García‐Marín, 2016b). Adaptive variants maintained by balancing selection have been reported in different species, such as those in immune‐related genes in three‐spined stickleback (Feulner et al., 2013; Guo et al., 2015) and in ribosomal structure and regulation genes in the albacore tuna (Laconcha et al., 2015). Seven of the eight outlier loci identified as being influenced by balancing selection in the current study were detected in the BAS‐BLS comparison, a result consistent with parallel adaptation to low salinities.…”

Geographical ancestry of Lake Malawi's cichlid fish diversity

“…In many cases, ancestors or sister species of these flocks have been identified, as with Galapagos finches [1], Hawaiian silverswords [2] and Canadian three-spined sticklebacks [3]. Identification of their origins has enabled discussion of events that initiated adaptive radiation, and allowed tests of whether diversification has been promoted by novel mutations that have arisen since colonization, or instead whether adaptation is based primarily on pre-existing genetic variation [4]. This is an important issue to resolve, because it can explain why only some colonizing lineages radiate when provided with ecological opportunity, and how parallel adaptive radiation can take place rapidly in geographically separated habitats.…”

Molecular ecology studies of species radiations: current research gaps, opportunities and challenges

“…With transcriptome and genome assemblies accumulating rapidly for many species and swift progress in the development of functional annotation tools, it seems that the time is now right for molecular ecologists to accept the challenge of studying radiations (as opposed to studying pairs or small groups of diverging taxa), thus building on theoretical advances in connecting micro-and macroevolutionary studies made in recent years (Salamin et al 2010;Smadja & Butlin 2012; The Marie Curie SPECIATION network 2011; Seehausen et al 2014;Simões et al 2016;Kostikova et al 2016). The role of transposable element (TE) dynamics (Brawand et al 2014), structural genomic (Feulner et al 2013) and epigenomic variation in fuelling radiations also represent highly promising avenues for future research. We look forward to seeing many exciting new studies of radiations that successfully bridge micro-and macroevolutionary approaches in the coming years.…”

“…They address some of the most hotly debated evolutionary radiations in animals and plants, including cichlids (e.g. Schliewen et al 2001;Colombo et al 2013;Keller et al 2013;Manousaki et al 2013;Albertson et al 2014;Ford et al 2015), sticklebacks (Gow et al 2006;Berner et al 2010;Deagle et al 2013;Feulner et al 2013), Anolis lizards (Glor et al 2005;Ng & Glor 2011;Muñoz et al 2013), Heliconius butterflies (Nadeau et al 2013), Darwin 0 s finches (Petren et al 2005), plants of the Hawaiian silversword alliance (Lawton-Rauh et al 2007), oak trees (Cavender-Bares et al 2015) and bromeliads (Palma-Silva et al 2011). Due to the targeted nature of our search and the specific search terms used, our literature review is certainly not exhaustive.…”