Mitochondrial sequence data indicate “Vicariance by Erosion” as a mechanism of species diversification in North American Ptomaphagus (Coleoptera, Leiodidae, Cholevinae) cave beetles

Abstract

Small carrion beetles (Coleoptera: Leiodidae: Cholevinae) are members of cave communities around the world and important models for understanding the colonization of caves, adaptation to cave life, and the diversification of cave-adapted lineages. We developed a molecular phylogeny to examine the diversification of the hirtus-group of the small carrion beetle genus Ptomaphagus. The hirtus-group has no surface-dwelling members; it consists of 19 short-range endemic cave- and soil-dwelling species in the central and southeastern United States of America. Taxonomic, phylogenetic and biogeographic data were previously interpreted to suggest the hirtus-group diversified within the past 350,000 years through a series of cave colonization and speciation events related to Pleistocene climate fluctuations. However, our time-calibrated molecular phylogeny resulting from the analysis of 2,300 nucleotides from five genes across three mitochondrial regions (cox1, cytb, rrnL-trnL-nad1) for all members of the clade paints a different picture. We identify three stages of diversification in the hirtus-group: (1) ~10 million years ago (mya), the lineage that develops into P.shapardi, a soil-dwelling species from the Ozarks, diverged from the lineage that gives rise to the 18 cave-obligate members of the group; (2) between 8.5 mya and 6 mya, seven geographically distinct lineages diverged across Kentucky, Tennessee, Alabama and Georgia; six of these lineages represent a single species today, whereas (3) the ‘South Cumberlands’ lineage in Tennessee and Alabama diversified into 12 species over the past ~6 my. While the events triggering diversification during the first two stages remain to be determined, the distributions, phylogenetic relationships and divergence times in the South Cumberlands lineage are consistent with populations being isolated by vicariant events as the southern Cumberland Plateau eroded and fragmented over millions of years.

Population genomics in two cave-obligate invertebrates confirms extremely limited dispersal between caves

“…The genus Ptomaphagus includes about 60 species in North America, again with roughly one third either troglophiles or troglobionts 4 . Diversification of the genus throughout the southern Cumberland Plateau is thought to have occurred through progressive vicariance, as the Cumberland Plateau eroded over the last 6 million years 19 . Like other troglobiotic Ptomaphagus, P. hatchi has greatly reduced eyes and is wingless.…”

“…Like other troglobiotic Ptomaphagus, P. hatchi has greatly reduced eyes and is wingless. On the southern Cumberland Plateau, N. barri and P. hatchi have largely overlapping ranges, with each species known from dozens of caves 12,19 , and both species are common in the caves they inhabit. Finally, where previous studies made use of one, or at most a handful loci, we take a genome-wide approach using 2bRAD 20 .…”

Testing the ‘caves as islands’ model in two cave-obligate invertebrates with a genomic approach

“…The genus Ptomaphagus includes about 60 species in North America, again with roughly one third either troglophiles or troglobionts (Peck 1986). Diversification of the genus throughout the southern Cumberland Plateau is thought to have occurred through progressive vicariance, as the Cumberland Plateau eroded over the last six million years (Leray et al 2019). Like other troglobiotic Ptomaphagus, P. hatchi has greatly reduced eyes and is wingless.…”

“…The southern Cumberland Plateau is one of the most cave-rich regions in North America, with more than 4000 caves known from a six-county area in southern Tennessee and northeast Alabama (Zigler et al 2014). On the southern Cumberland Plateau, N. barri and P. hatchi have largely overlapping ranges, with each species known from dozens of caves (Snowman et al 2010;Leray et al 2019), and both species are common in the caves they inhabit. Finally, where previous studies made use of one, or at most a handful loci, we take a genome wide approach using 2bRAD (Wang et al 2012).…”

Morphometrics and phylogeography of the cave-obligate land snail Helicodiscus barri (Gastropoda, Stylommatophora, Helicodiscidae)

“…Cave systems, characterized by geographic isolation and relatively simple biological communities, often are viewed as analogous to oceanic islands (Culver andPipan 2009, Snowman et al 2010). Strong selective pressures and the isolation of subterranean ecosystems can result in morphological stasis among otherwise genetically distinct species, largely due to the parallel or convergent evolution of these lineages (Lefébure et al 2006, Finston et al 2007, Niemiller et al 2012. Further, many troglobites (i.e., terrestrial cave-obligates) exhibit broad, mosaic distribution patterns which, in conjunction with morphological stasis, often confound traditional approaches of delimitating species boundaries (Jochum et al 2015).…”