Ancient lineage, young troglobites: recent colonization of caves by Nesticella spiders

Yuanyuan Zhang,Shuqiang Li

doi:10.1186/1471-2148-13-183

Abstract

BackgroundThe evolution and origin of cave organisms is a recurring issue in evolutionary studies, but analyses are often hindered by the inaccessibility of caves, morphological convergence, and complex colonization processes. Here we investigated the evolutionary history of Nesticella cave spiders, which are mainly distributed in the Yunnan–Guizhou Plateau, China. With comprehensive sampling and phylogenetic and coalescent-based analyses, we investigated the tempo and mode of diversification and the origins of these troglobites. We also aimed to determine which factors have influenced the diversification of this little-known group.ResultsCoalescent-based species delimitation validated the 18 species recognized by morphological inspection and also suggested the existence of cryptic lineages. Divergence time estimates suggested that Nesticella cave spiders in the Yunnan–Guizhou Plateau constituted a monophyletic troglobite clade that originated in the middle Miocene (11.1–18.6 Ma). Although the Yunnan–Guizhou Plateau clade was composed exclusively of troglobite species, suggesting an ancient common subterranean ancestor, we favor multiple, independent cave colonizations during the Pleistocene over a single ancient cave colonization event to explain the origin of these cave faunas. The diversification of plateau Nesticella has been greatly influenced by the sequential uplift of the plateau and likely reflects multiple cave colonizations over time by epigean ancestors during Pleistocene glacial advances.ConclusionsWe concluded that plateau cave Nesticella represent an ancient group of spiders, but with young troglobite lineages that invaded caves only recently. The absence of extant epigean relatives and nearly complete isolation among caves supported their relict status. Our work highlights the importance of comprehensive sampling for studies of subterranean diversity and the evolution of cave organisms. The existence of potentially cryptic species and the relict status of Nesticella highlight the need to conserve these cave spiders.

Highlights

The evolution and origin of cave organisms is a recurring issue in evolutionary studies, but analyses are often hindered by the inaccessibility of caves, morphological convergence, and complex colonization processes
Best-fit models selected by jModelTest were TrN + I + G for cox1, TPMuf + I + G for 12S/16S, TPM1 + I for histone 3 gene (H3), TrN + G for 28S, and TrNef + G for 18S
Using a multilocus species tree method for divergence time estimates, we found that the plateau Nesticella cave spiders constituted a monophyletic clade that originated in the early Miocene

Summary

Introduction

The evolution and origin of cave organisms is a recurring issue in evolutionary studies, but analyses are often hindered by the inaccessibility of caves, morphological convergence, and complex colonization processes. Especially terrestrial invertebrates, adapted to cave environments are often reported to be highly geographically isolated, because of their limited dispersal ability resulting from limited physiological tolerances [8,9,10]. Their spatial isolation, The competing climate-relict and adaptive-shift hypotheses have been proposed to explain the origins of cave organisms [3]. The adaptive-shift model supposes that pre-adapted epigean species actively colonized caves to exploit novel resources and diverged under a gene flow scenario [13,14]. Divergent selection among epigean and subterranean habitats gradually overcame the homogenizing process of gene flow and eventually led to parapatric speciation [15]

Methods

Results

Discussion

Conclusion