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

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.

Heat tolerance and acclimation capacity in subterranean arthropods living under common and stable thermal conditions

“…Taken together, these results suggest that maintaining heat tolerance beyond the range of temperatures experienced, as well as some degree of thermal plasticity, could be less costly than a priori expected in a constant, stable, and resource‐limiting environment such as caves. Caves are environments with extreme selection pressures and adapted organisms that are similar in appearance, physiology, and behavior all over the world, despite their different origins (Howarth & Moldovan, ; Liu et al, ; Trontelj, Blejec, & Fišer, ). However, our results show that upper thermal limits and acclimation capacities are not so homogeneous across subterranean invertebrates cohabiting the same cave, suggesting a weak role of thermal stability as a selective pressure on heat tolerance traits.…”

“…The target species belong to three different orders of arthropods: (a) Glomeris sp. (Diplopoda: Glomerida: Glomeridae) is an undescribed species of a mega‐diverse genus within the order Glomerida (Golovatch, Mauriès, Akkari, Stoev, & Geoffroy, ) confined to some caves in South Spain (unpublished observations), which shows well‐developed troglomorphic traits (depigmentation, reduced thickness of tergites, reduced ocelli, and elongation of body and appendages, see Liu, Golovatch, Wesener, & Tian, ); (b) Deuteraphorura silvaria (Gisin, 1952) (Entognatha: Collembola: Onychiuridae) is distributed in Central and South Europe (Arbea, , ); (c) Speonemadus angusticollis (Kraatz, 1870) (Coleoptera: Leiodidae) is an Iberian endemic species, and (d) Atheta subcavicola (Brisout de Barneville, 1863) (Coleoptera: Staphylinidae) is one of the few species of the genus Atheta associated with caves (Assing & Vogel, ), distributed in the Iberian Peninsula and France (Balazuc, Miré, Sigwalt, & Théodoridès, ; Barranco et al, ; Reboleira, Gonçalves, & Oromí, ). The four species are usually found close to guano deposits in the study cave, but show different degrees of subterranean specialization.…”

Four new species of the millipede genus Eutrichodesmus Silvestri, 1910 from Laos, including two with reduced ozopores (Diplopoda, Polydesmida, Haplodesmidae)

“…The function of the defensive glands and their ozopores is known to lie in the production of defence fluids, as a protection against predators (Shear 2015). From the recent paper concerning the adaptation in the cave millipedes to the cave environment (Liu et al 2017) it remains unclear whether or not the suppression may be related to cavernicoly. We are rather inclined to think it is not.…”

The troglomorphic adaptations of Namanereidinae (Annelida, Nereididae) revisited, including a redescription of Namanereis cavernicola (Solís-Weiss & Espinasa, 1991), and a new Caribbean species of Namanereis Chamberlin, 1919

“…For example, the elongation of some segments of legs seems to be unique among stygobiont millipedes, but not the elongation of antennae (Liu et al 2017). On the other hand, Delić et al (2016: 46) found for the stygobiont amphipod Niphargus croaticus (Jurinac, 1887) that elongation in legs is more related with local factors as low of absent water flow and interspecific competition, rather than food availability or time of colonization; moreover, they found a high differentiation among closely related populations, suggesting a fast morphological change regarding this feature (p. 46).…”