Evolutionary Dynamics of Structural Variation at a Key Locus for Color Pattern Diversification in Cichlid Fishes

Abstract

Color patterns in African cichlid fishes vary spectacularly. Although phylogenetic analysis showed already 30 years ago that many color patterns evolved repeatedly in these adaptive radiations, only recently have we begun to understand the genomic basis of color variation. Horizontal stripe patterns evolved and were lost several times independently across the adaptive radiations of Lake Victoria, Malawi, and Tanganyika and regulatory evolution of agouti-related peptide 2 (agrp2/asip2b) has been linked to this phenotypically labile trait. Here, we asked whether the agrp2 locus exhibits particular characteristics that facilitate divergence in color patterns. Based on comparative genomic analyses, we discovered several recent duplications, insertions, and deletions. Interestingly, one of these events resulted in a tandem duplication of the last exon of agrp2. The duplication likely precedes the East African radiations that started 8–12 Ma, is not fixed within any of the radiations, and is found to vary even within some species. Moreover, we also observed variation in copy number (two to five copies) and secondary loss of the duplication, illustrating a surprising dynamic at this locus that possibly promoted functional divergence of agrp2. Our work suggests that such instances of exon duplications are a neglected mechanism potentially involved in the repeated evolution and diversification that deserves more attention.

Developmental and Cellular Basis of Vertical Bar Color Patterns in the East African Cichlid Fish Haplochromis latifasciatus

“…On the other hand, a gradient in agrp2 expression along anterio-posterior axis could be found in both H. latifasciatus with significant difference from this study ( Figure 5J and Supplementary Table S2) and P. nyererei without significant difference from our previous study (Kratochwil et al, 2018). However, based on our previous work that showed no changes in bar patterns in a knockout of agrp2 in P. nyererei (Kratochwil et al, 2018) or association with bar presence and absence (Kratochwil et al, 2019a), a role in vertical bar formation seems rather unlikely.…”

Different Sources of Allelic Variation Drove Repeated Color Pattern Divergence in Cichlid Fishes

“…Baits were designed from the P. nyererei reference genome ( Brawand et al. 2014 ) which was curated by filling gaps of the genome assembly using Sanger sequencing reads so that the modified genome now contains the “stripe interval” ( Kratochwil et al. 2019 ).…”

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

“…the contribution of inversions to speciation events, as highlighted by previous studies [37][38][39][40]; the role of SVs in shaping the expression landscape by altering gene sequences, gene copy number, or regulatory elements [66][67][68][69]; further studies on SV identification, evolution and biological role, considering a different (and possibly greater) set of species .The inclusion of data from additional species, and the resolution of intra and inter specific variability would result in a much greater power in reconstructing the evolutionary dynamics of each SV event [34,70]. Moreover, it would facilitate the identification of any association between SVs and traits under selection.…”

“…Gene or exon duplication events might lead to neo-or subfunctionalisation [29][30][31][32][33]. Recently, an evolutionary study in East African cichlids focusing on agrp2 (a locus controlling horizontal stripe patterns) revealed several recent duplications, insertions, and deletions, including a tandem duplication of the last exon [34]. This event is not fixed in any of the radiations, and is polymorphic even within some species.…”