Can species endure massive introgression? Genomic evidence of asymmetric gene flow in Melitaea butterflies

• Published in: Systematic entomology 2024-10, Vol.49 (4), p.583-595
• Main Authors: Hinojosa, Joan C., Marques, Valéria, Mesa, Luis Sánchez, Dapporto, Leonardo, Dincă, Vlad, Vila, Roger
• Format: Article
• Language: English
• Subjects: ddRADseq; Evolution; Gene flow; Genomics; hybridisation; Interspecific hybridization; introgression; Lepidoptera; Melitaea; Metallura phoebe; Phenotypes; phylogeography; Somatic chromosomes; Voltinism; Z chromosomes
• ISSN: 0307-6970; 1365-3113
• DOI: 10.1111/syen.12631

Hybridisation and introgression are increasingly seen as important drivers of the evolution of organisms, particularly in Lepidoptera. One group that is gaining attention due to recently published cases of interspecific gene flow is the genus Melitaea Fabricius (Nymphalidae). In this study, we used genomics to investigate the role of hybridisation in the evolution of the western Palearctic species of the Melitaea phoebe group M. ornata Christoph, the recently described M. pseudornata Muñoz Sariot & Sánchez Mesa, M. phoebe (Denis & Schiffermüller), M. punica Oberthür, and M. telona (Fruhstorfer). We provide evidence of asymmetric gene flow from M. phoebe to both M. ornata and M. pseudornata. Gene flow from M. phoebe to M. pseudornata was very high (25.0%–31.9%), widespread throughout the distribution of the latter, and not equally distributed along the genome. The Z chromosome showed patterns compatible with the large‐Z effect, which were mimicked by two autosomes. Melitaea pseudornata endured massive introgression while remaining a separate entity from M. phoebe, although gene flow may have altered its phenotype, including its voltinism and the morphology of the adults and caterpillars. These findings suggest that hybridisation may be pervasive in this genus and highlight its key role in the evolution of butterflies, emphasising the need for further research on this topic. We provide evidence of asymmetric gene flow from Melitaea phoebe to M. ornata and, especially, to M. pseudornata, for which gene flow may have affected a high proportion of its genome. Gene flow was not equally distributed along the genome: the Z chromosome showed patterns compatible with the large‐Z effect. As a result of the genetic interchange with M. phoebe, the phenotype of M. pseudornata, including its voltinism and morphology, has been potentially altered.