Evolutionary transition from surface to subterranean living in Australian water beetles (Coleoptera: Dytiscidae) through adaptive and relaxed selection

Abstract

Over the last 5 million years, numerous species of Australian stygobiotic (subterranean and aquatic) beetles have evolved underground following independent colonization of aquifers by surface ancestors, providing a set of repeated evolutionary transitions from surface to subterranean life. We used this system as an ‘evolutionary experiment’ to investigate whether relaxed selection has provided a source of variability for adaptive radiations into ecosystems containing open niches and whether this variability underpins phenotypic evolution in cave animals. Linear and landmark-based measurements were used to quantify the morphology of subterranean species from different aquifers, compared to interstitial and closely related aquatic surface species. Subterranean dytiscids were observed to be morphologically distinct, suggesting they have a different lifestyle compared to their surface relatives. However, variation in the measured traits was much greater in the subterranean species, and unstructured, showing no evidence of clustering that would indicate adaptation to specific niches. Furthermore, a previously identified pattern of repeated nonoverlapping size variation in beetles across aquifers was not correlated with repeated body shape evolution. The observed variability across body shape and limb traits provides support for the hypothesis that relaxed selection and neutral evolution underlie the phenotypic evolution in these species.

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

“…These aquatic beetle tribes underwent underground colonization more recently (ca. 7–3 Mya) and show clear phenotypic differences between surface-dwelling and subterranean species (Leijs et al 2012; Langille et al 2021; Zhao et al 2023). The chemosensory gene repertoire has been characterized so far in a single cave species, the Leptodirini beetle Speonomus longicornis .…”