Analysis of structural variants in four African Cichlids highlights an association with developmental and immune related genes

Abstract

Background . East African lake cichlids are one of the most impressive examples of an adaptive radiation. Independently in Lake Victoria, Tanganyika, and Malawi, several hundreds of species arose within the last 10 million to 100,000 years. Whereas most analyses in cichlids focused on nucleotide substitutions across species to investigate the genetic bases of this explosive radiation, to date, no study has investigated the contribution of structural variants (SVs) in the evolution of adaptive traits across the three Great Lakes of East Africa. Results . Here, we annotate and characterize the repertoires and evolutionary potential of different SV classes (deletion, duplication, inversion, insertions and translocations) in four cichlid species: Haplochromis burtoni, Metriaclima zebra, Neolamprologus brichardi and Pundamilia nyererei . We investigate the patterns of gain and loss evolution for each SV type, enabling the identification of lineage specific events. Both deletions and inversions show a significant overlap with SINE elements, while inversions additionally show a limited, but significant association with DNA transposons. Inverted regions are enriched for genes regulating behaviour, or involved in skeletal and visual system development. We also find that duplicated regions show enrichment for genes associated with "antigen processing and presentation" and other immune related categories. Our pipeline and results were further tested by PCR validation of selected deletions and inversions, which confirmed respectively 7 out of 10 and 6 out of 9 events. Conclusions . Altogether, we provide the first comprehensive overview of rearrangement evolution in East African cichlids, and some important insights into their likely contribution to adaptation. BackgroundAfrican cichlids represent one of the best examples of rapid adaptive radiation [1][2][3][4]. The adaptation to different ecological niches in Lakes Malawi, Tanganyika and Victoria has given rise to several hundreds of species in a period of just a few million years [5][6][7]. The radiation is associated with great phenotypic variation, including jaw morphology, body shape, coloration, adaptation of the visual system to different water depths, and behavior [8][9][10][11][12][13][14][15][16]. Variation in ecological niches and behaviour appears to be associated with different brain development [17], with differences appearing already at early developmental stages [18]. A great example of adaptation is represented by the evolution of the 3 cichlid visual system, involving eight different opsin genes [19][20][21].To gain insights on the molecular mechanisms underlying this rapid radiation, Brawand et al. [22] generated genome references for five species: the Nile tilapia (Oreochromis niloticus), representing an ancestral lineage; Neolamprologus brichardi (Lake Tanganyika), Metriaclima zebra (Lake Malawi), Pundamilia nyererei (Lake Victoria), and Haplochromis burtoni (riverine species around Lake Tanganyika). The study highlighted several mechanisms underlyin...