Highly dynamic evolution of the chemosensory system driven by gene gain and loss across subterranean beetles.

Chemical cues in subterranean habitats differ highly from those on the surface due to the contrasting environmental conditions, such as absolute darkness, high humidity or food scarcity. Subterranean animals underwent changes to their sensory systems to facilitate the perception of essential stimuli for underground lifestyles. Despite representing unique systems to understand biological adaptation, the genomic basis of chemosensation across cave-dwelling species remains unexplored from a macroevolutionary perspective. Here, we explore the evolution of chemoreception in three beetle tribes that underwent at least six independent transitions to the underground, through a phylogenomics spyglass. Our findings suggest that the chemosensory gene repertoire varies dramatically between species. Overall, no parallel changes in the net rate of evolution of chemosensory gene families were detected prior, during, or after the habitat shift among subterranean lineages. Contrarily, we found evidence of lineage-specific changes within surface and subterranean lineages. However, our results reveal key duplications and losses shared between some of the lineages transitioning to the underground, including the loss of sugar receptors and gene duplications of the highly conserved ionotropic receptors IR25a and IR8a, involved in thermal and humidity sensing among other olfactory roles in insects. These duplications were detected both in independent subterranean lineages and their surface relatives, suggesting parallel evolution of these genes across lineages giving rise to cave-dwelling species. Overall, our results shed light on the genomic basis of chemoreception in subterranean beetles and contribute to our understanding of the genomic underpinnings of adaptation to the subterranean lifestyle at a macroevolutionary scale.

Parallel and convergent genomic changes underlie independent subterranean colonization across beetles.

Adaptation to life in caves is often accompanied by dramatically convergent changes across distantly related taxa, epitomized by the loss or reduction of eyes and pigmentation. Nevertheless, the genomic underpinnings underlying cave-related phenotypes are largely unexplored from a macroevolutionary perspective. Here we investigate genome-wide gene evolutionary dynamics in three distantly related beetle tribes with at least six instances of independent colonization of subterranean habitats, inhabiting both aquatic and terrestrial underground systems. Our results indicate that remarkable gene repertoire changes mainly driven by gene family expansions occurred prior to underground colonization in the three tribes, suggesting that genomic exaptation may have facilitated a strict subterranean lifestyle parallelly across beetle lineages. The three tribes experienced both parallel and convergent changes in the evolutionary dynamics of their gene repertoires. These findings pave the way towards a deeper understanding of the evolution of the genomic toolkit in hypogean fauna.

Rudogorites simonei gen. nov. and sp. nov. from Central Bosnia (Coleoptera: Leiodidae: Cholevinae: Leptodirini).

Dinaric karst in Western Balkans is especially biodiverse in cave beetle fauna. Despite the territory of Bosnia and Herzegovina being a relatively well-studied region, new species are still discovered and described regularly, even in recent times. Discoveries of new genera are, however, rare. Based on recently collected beetle specimens in the cave Lijina Peina near the town of Kreevo in the region of Bosansko Rudogorje in Central Bosnia, a new troglobiotic leptodirine genus Rudogorites gen. nov. and a single new species R. simonei sp. nov. are described. The region of Bosansko Rudogorje consists mainly of non-carbonate rocks, sandstones and polymetallic ore. In the area, there is a patch of isolated karst where a new endemic subterranean fauna has been found. An updated key to the Leptodirini genera of the Apholeuonus phyletic group is provided.

Aphaenogasterillyrica, a new species from the mountains of the Balkan Peninsula (Hymenoptera, Formicidae).

Aphaenogasterillyrica sp. nov., a member of the A.subterranea species group, is described from Dinaric Alps of Slovenia and Croatia, from Golesnica Mt. in north Macedonia, Osogovo-Belasica Massif of southwestern Bulgaria, and from Kerkini Mts. of Greek Macedonia. It is characterised by large body size, moderately sculptured head, elevated mesonotum, and long propodeal spines. Its habitat preferences are discussed. A key to the Aphaenogastergraeca complex is provided.