The genomics of convergent adaptation to intertidal gravel beaches in Mediterranean clingfishes

Abstract

IntroductionUnderstanding the genetic basis of widespread phenotypic convergence, particularly for complex morphological traits, remains a major challenge in evolutionary biology. The Mediterranean gravel beach clingfishes of the genus Gouania provide an excellent system to study this phenomenon. Within this genus, two distinct morphotypes, "slender" and "stout", have repeatedly evolved, adapting to different microhabitats. These morphotypes differ in multiple complex traits, including body elongation, head compression, vertebral number, eye size, and the structure of the adhesive disc. Materials and MethodsIn a first step, to scrutinize phylogenetic convergence, we combined 3D morphometrics of the pelvic girdle and skull, with molecular species delimitation based on >660 DNA barcodes, and a phylogenomic framework based on more than 3,400 single-copy orthologs. Secondly, by employing whole-genome resequencing and a novel "convergence score" statistic, we examined genomic convergence across multiple levels: nucleotides, sequences, genes, and functional pathways. Results and DiscussionWhile we found no evidence of large-scale genomic or protein-level convergence, we identified promising candidate regions at the level of single variants, genes, and biological pathways. Notably, a longer shared (but interrupted) haplotype around the morphogene adam12 was associated with convergent traits. The lack of simple genomic patterns may reflect the radiations age and the complex genetic basis of the underlying morphological traits (e.g., eye-size, neurocranium shape). Altogether, our findings highlight the importance of assessing genomic convergence at multiple molecular levels to uncover diagnostic signals across varying evolutionary processes and timescales. GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=149 SRC="FIGDIR/small/675783v1_ufig1.gif" ALT="Figure 1"> View larger version (61K): org.highwire.dtl.DTLVardef@58265eorg.highwire.dtl.DTLVardef@13f1deaorg.highwire.dtl.DTLVardef@c51d79org.highwire.dtl.DTLVardef@112217d_HPS_FORMAT_FIGEXP M_FIG C_FIG