Behavioural foundation of a massive mitochondrial introgression in the fire salamander, Salamandra salamandra

Abstract

Patterns of mito-nuclear discordance across secondary contact zones have been reported in a wide range of animal and plant organisms. They consist of a spatial mismatch between nuclear and mitochondrial genomes, in terms of the geographic location and/or extension of the secondary contact zone between distinct evolutionary lineages. Several theoretical and empirical studies have identified massive mitochondrial introgression as the putative source of these mismatches. Yet, we still lack a clear understanding of the potential phenotypic underpinnings of these instances of massive introgression. In this study, we addressed the hypothesis that mtDNA variation across a contact zone could be associated with variation at phenotypic traits affecting dispersal propensity. We analyzed patterns of behavioural and genetic variation across a mtDNA secondary contact zone of the fire salamander Salamandra salamandra in central Italy, which is over 600 km displaced from its nuclear counterpart. We found distinct behavioral profiles associated with the two mitotypes co-occurring in the mtDNA secondary contact zone. Counterintuitively, we found a slow-thorough dispersal profile associated with the massively introgressed mitotype. This dispersal profile was characterized by shy, less active and less exploratory personality traits, and this pattern was consistent across life-stages and contexts (i.e., aquatic larvae and terrestrial juveniles). Our results provide experimental evidence supporting the intriguing hypothesis that personality traits associated with distinct mitotypes could promote differential mitochondrial introgression within alternative nuclear backgrounds.