Disentangling the evolutionary history of peri-Mediterranean cyprinids using host-specific gill monogeneans

Abstract

The diversification of Mediterranean fish appears to be far more complex than could be explained by a single dispersion model. Cyprinids represent one of the most species-rich groups of freshwater fishes living in this region. The current distribution of several highly divergent cyprinid taxa is most likely the result of multiple dispersion events. Cyprinid fish serve as hosts for the highly diversified and host-specific monogenean parasites of the genus Dactylogyrus. On the assumption that the distribution of Dactylogyrus spp. reflects the biogeography and evolutionary history of their hosts, we used these parasites as an additional tool to shed new light on the evolutionary history of peri-Mediterranean cyprinids of the subfamily Barbinae. The degree of congruence between host and parasite phylogenies was investigated using 29 Dactylogyrus spp. and 34 Barbinae hosts belonging to the genera Aulopyge, Barbus and Luciobarbus. We showed that the morphological adaptation of Dactylogyrus (i.e. of the ventral bar, representing the most variable morphological character of the attachment organ) is linked with parasite phylogeny. By applying distance-based and event-based cophylogenetic approaches, we revealed a significant global coevolutionary signal. A total of 62% of individual host–parasite links contributed significantly to the coevolutionary structure evidenced between hosts of Barbus spp. and Iberian Luciobarbus spp., and their host-specific Dactylogyrus spp. The host switching of parasites was revealed as the most important coevolutionary event in the Dactylogyrus-Barbinae system in the peri-Mediterranean region. Cophylogenetic analyses and the mapping of the morphological character of the parasite attachment organ onto the phylogeny of Dactylogyrus indicate that endemic southern European Dactylogyrus spp. parasitizing cyprinids of Barbinae have multiple origins. We suggest that continental bridges connecting southern Europe and North Africa played a crucial role in the dispersion of cyprinids, affecting the distribution of their host-specific gill parasites.