Convergent Evolution of Unique Morphological Adaptations to a Subterranean Environment in Cave Millipedes (Diplopoda).

Mingyi Tian,Weixin Liu,Thomas Wesener,Claude Wicker-Thomas,Sergei Golovatch

doi:10.1371/journal.pone.0170717

Abstract

Animal life in caves has fascinated researchers and the public alike because of the unusual and sometimes bizarre morphological adaptations observed in numerous troglobitic species. Despite their worldwide diversity, the adaptations of cave millipedes (Diplopoda) to a troglobitic lifestyle have rarely been examined. In this study, morphological characters were analyzed in species belonging to four different orders (Glomerida, Polydesmida, Chordeumatida, and Spirostreptida) and six different families (Glomeridae, Paradoxosomatidae, Polydesmidae, Haplodesmidae, Megalotylidae, and Cambalopsidae) that represent the taxonomic diversity of class Diplopoda. We focused on the recently discovered millipede fauna of caves in southern China. Thirty different characters were used to compare cave troglobites and epigean species within the same genera. A character matrix was created to analyze convergent evolution of cave adaptations. Males and females were analyzed independently to examine sex differences in cave adaptations. While 10 characters only occurred in a few phylogenetic groups, 20 characters were scored for in all families. Of these, four characters were discovered to have evolved convergently in all troglobitic millipedes. The characters that represented potential morphological cave adaptations in troglobitic species were: (1) a longer body; (2) a lighter body color; (3) elongation of the femora; and (4) elongation of the tarsi of walking legs. Surprisingly, female, but not male, antennae were more elongated in troglobites than in epigean species. Our study clearly shows that morphological adaptations have evolved convergently in different, unrelated millipede orders and families, most likely as a direct adaptation to cave life.

Highlights

Caves represent one of the world’s most intriguing ecosystems [1,2], as, unlike surface habitats, they are completely devoid of sunlight, with neither photosynthesis nor plant growth, and have constant, usually much cooler temperatures and a limited food supply [3].The cave environment is often separated into a twilight zone near the entrance, a middle zone of complete darkness with variable temperature, and a zone of complete darkness withPLOS ONE | DOI:10.1371/journal.pone.0170717 February 8, 2017Cave Adaptations in Millipedes nearly constant temperature in the deep interior [2]
Epigean sister taxa to the troglobitic species would have been included; no phylogeny for our investigated genera is available, we note that the morphological characters utilized here show very little interspecific variation among congeneric epigean species, and most were not even mentioned in taxonomic descriptions [66,79,91,92,98]
Golovatch and Enghoff [72] mentioned that the maximal width of antennomere 6 and the length/width ratio of the Tomosvary organ might represent potential synapomorphy of the Glomeris alluaudi group, which contains several presumed troglobites, on the Canary Islands

Summary

Introduction

Cave Adaptations in Millipedes nearly constant temperature in the deep interior [2]. The latter area is considered as the “true cave area” [4]. Each cave ecosystem is unique and often quite fragile; the peculiar cave-dwelling fauna are often characterized by their extreme scarcity and high endemism to a specific cave at the species level. The isolation and distinctiveness of each individual cave ecosystem, in combination with the locally evolved endemic cave species (troglobites: obligate cavernicoles), make caves important habitats for research in evolutionary adaptations [5,6]

Methods

Results

Conclusion