Phylogeography of Sarmarutilus rubilio (Cypriniformes: Leuciscidae): Complex Genetic Structure, Clues to a New Cryptic Species and Further Insights into Roaches Phylogeny.

Italy hosts a large number of endemic freshwater fish species due to complex geological events which promoted genetic differentiation and allopatric speciation. Among them, the South European roach Sarmarutilus rubilio inhabits various freshwater environments in three different ichthyogeographic districts. We investigated the genetic diversity of S. rubilio using two different mitochondrial markers (COI and CR), aiming to define its relationship with other similar taxa from the Balkan area and, from a phylogeographic perspective, test the effects of past hydrogeological dynamics of Italian river basins on its genetic structure and demographic history. Our analysis highlighted a marked genetic divergence between S. rubilio and all other roach species and, among Italian samples, revealed the existence of three deeply divergent geographic haplogroups, named A, B and C. Haplogroup C likely corresponds to a new putative cryptic species and is located at the northern border of the South European roach range; haplogroup B is restricted to Southern Italy; and haplogroup A is widespread across the entire range and in some sites it is in co-occurrence with C or B. Their origin is probably related to the tectonic uplifting of the Apuan Alps in the north and of the Colli Albani Volcano in the south during the Pleistocene, which promoted isolation and vicariance followed by secondary contacts.

Balancing selection, genetic drift, and human-mediated introgression interplay to shape MHC (functional) diversity in Mediterranean brown trout.

The extraordinary polymorphism of major histocompatibility complex (MHC) genes is considered a paradigm of pathogen-mediated balancing selection, although empirical evidence is still scarce. Furthermore, the relative contribution of balancing selection to shape MHC population structure and diversity, compared to that of neutral forces, as well as its interaction with other evolutionary processes such as hybridization, remains largely unclear. To investigate these issues, we analyzed adaptive (MHC-DAB gene) and neutral (11 microsatellite loci) variation in 156 brown trout (Salmo trutta complex) from six wild populations in central Italy exposed to introgression from domestic hatchery lineages (assessed with the LDH gene). MHC diversity and structuring correlated with those at microsatellites, indicating the substantial role of neutral forces. However, individuals carrying locally rare MHC alleles/supertypes were in better body condition (a proxy of individual fitness/parasite load) regardless of the zygosity status and degree of sequence dissimilarity of MHC, hence supporting balancing selection under rare allele advantage, but not heterozygote advantage or divergent allele advantage. The association between specific MHC supertypes and body condition confirmed in part this finding. Across populations, MHC allelic richness increased with increasing admixture between native and domestic lineages, indicating introgression as a source of MHC variation. Furthermore, introgression across populations appeared more pronounced for MHC than microsatellites, possibly because initially rare MHC variants are expected to introgress more readily under rare allele advantage. Providing evidence for the complex interplay among neutral evolutionary forces, balancing selection, and human-mediated introgression in shaping the pattern of MHC (functional) variation, our findings contribute to a deeper understanding of the evolution of MHC genes in wild populations exposed to anthropogenic disturbance.