Colonization patterns of epi- and endogenous habitats suggest extrinsic and intrinsic drivers to cavernicoly on Réunion island by Cixiidae (Hemiptera, Fulgoromorpha)

Abstract The study focuses on the evolutionary and taxonomic dynamics driving cavernicoly (cave-dwelling behavior) within Cixiidae planthoppers on La Réunion Island. A comprehensive phylogenetic analysis of the island’s cixiid species reveals that the genus Brixia , the most diversified cixiid taxon on the island, exhibits both epigean and hypogean adaptations. In particular, the lalouettei + clade includes eutroglophile species, with two independently evolved troglobiont species, Brixia briali and Brixia sp. nov., while its sister clade includes only epigean species. Several potential cryptic species are disclosed, particularly within the genera Brixia and Achaemenes . Overall, and corresponding to each genus of Cixiidae present in La Réunion, a minimum of five independent dispersal events must be considered, with potentially even two separate events for the genera Brixia and Achaemenes . In light of the phylogenetic framework obtained, we address the drivers behind cavernicoly in these taxa, focusing on the interplay between external ecological pressures and intrinsic genetic factors. We show that Howarth’s adaptive shift hypothesis, suggesting that species actively colonized caves as new ecological niches being available, aligns well with the observed phylogenetic pattern of close relative species present. However, Vandel’s “climatic relict” hypothesis cannot be discarted in relation with unfavorable surface conditions some 21,000 years ago during the Last Glacial Maximum in La Reunion, that may have pushed epigean species underground. These two processes may not be mutually exclusive. The combination of life traits such as underground feeding behavior on roots, possible relaxed dietary preferences of island taxa, and the weaker defense systems of secondary roots in caves, likely facilitated the adaptation of Brixia species to cave environments. However, if these traits may be viewed as exaptations that enabled these taxa to successfully transition to cavernicolous lifes traits, the phylogenetic-based divergence between a strictly epigean costalis + group and and its eutroglophile sister clade lalouettei+ , suggests that some genetic factors may also play a critical role in supporting cavernicoly.