Convergent Reduction of Ovariole Number Associated with Subterranean Life in Beetles

PLoS One. 2015 Jul 7;10(7):e0131986. doi: 10.1371/journal.pone.0131986. eCollection 2015.

Abstract

Background: Some species of obligate cavernicolous beetles are known to possess a unique feature-a contraction of the larval cycle. In contrast to many other subterranean beetles, life-cycle contraction in Trechini ground beetles (Carabidae) is correlated with a reduction in the number of eggs and a drastic reduction in the number of ovarioles. This remarkable peculiarity has only been reported for a small number of closely related species.

Results: We give a description of the female internal reproductive system for six species of Trechini, including five subterranean species, with a particular focus on the western Pyrenean radiation of Aphaenops, a group for which nothing is known regarding the early life stages. We redescribe the internal female genitalia of A. crypticola Linder. Study of the ovarioles allowed us to infer the postembryonic development of the larvae for each species examined. We then used a phylogenetic framework to recognize two independent reductions in the number of ovarioles in the Pyrenean lineage. We discuss the multiple convergent evolutions in ovariole number and the potential link between a reduction of ovariole number and troglobiomorphism in a phylogenetic context.

Conclusions: There is an extreme reduction in ovariole number and size within the species studied; the eggs produced by small ovarioles have a remarkably large size. A reduction to one ovariole has occurred independently at least twice in this subterranean group. A reduction in the number of ovarioles in ground beetles is one of the striking consequences of subterranean specialization and it is correlated with another remarkable adaptation of subterranean beetles, a reduction in the number of larval instars.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Coleoptera / classification
  • Coleoptera / growth & development
  • Coleoptera / physiology*
  • DNA, Mitochondrial / analysis
  • Ecosystem
  • Female
  • Larva / growth & development
  • Life Cycle Stages
  • Oocytes / growth & development
  • Ovary / anatomy & histology
  • Ovary / growth & development*
  • Phylogeny

Substances

  • DNA, Mitochondrial

Grants and funding

This work has been funded by a German Research Foundation project to AF (FA 1042/1-1). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.