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

Introduction

Understanding 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 Methods

In 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 Discussion

While 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 radiation’s 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