Cytonuclear incongruences hamper species delimitation in the socially polymorphic desert ants of the Cataglyphis albicans group in Israel

Abstract

Assessing whether behavioural, ecological or geographical factors trigger population divergence provides key insights into the biological processes driving speciation. Recent speciation in restricted geographic area without obvious ecological barriers prompts the question of the behavioural mechanisms underlying species divergence. In this context, we investigated phylogenetic relationships in the Cataglyphis albicans desert ant complex in Israel. We first determined accurate species delimitation using two mitochondrial and six nuclear genes, as well as 11 microsatellite markers to investigate cryptic species in this group, assessing reduction in gene flow between populations. We then investigated whether different species in this group exhibit distinct reproductive strategies, inferring social structure and queen-mating frequency in each species uncovered. Our findings highlight the presence of at least six distinct Cataglyphis albicans species in the restricted range of Israel; four of them co-occur in a 50 × 50 km area in North Negev, while two are endemic from there. However, our results reveal incongruences between nuclear and mitochondrial clustering, which complicate species identification and preclude the exclusive use of mtDNA to confidently delimit species in this group. Finally, we show that the different species of the C. albicans group in Israel exhibit quite similar reproductive strategies with most of them having colonies headed by a single queen mated with several males; colonies of one species were, however, headed by several queens. Overall, this weak variation across species thereby unlikely represents the main evolutionary force behind speciation of these sympatric species. We then discuss the potential evolutionary processes that underlie speciation in this group in the absence of clear geographical or ecological barriers.