Ancient associations of aquatic beetles and tank bromeliads in the Neotropical forest canopy

*Zoological State Collection, Muenchhausenstrasse 21, 81247 Munich, Germany;
^†Department of Entomology, The Natural History Museum, London SW7 5BD, United Kingdom;
^§Institut de Biologia Molecular de Barcelona, Centre d'Investigació i Desenvolupament–Consell Superior d'Investigacions Científiques, Jordi Girona 18-26, 08034 Barcelona, Spain;
^¶Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, José Gutiérrez Abascal 2, 28006 Madrid, Spain;
^‖Centro de Ecología, Instituto Venezolano de Investigaciones Científicas, Apartado Postal 21827, Caracas 1020-A, Venezuela;
**Zoologisches Institut, Universität Tübingen, Ob dem Himmelreich 7, 72076 Tübingen, Germany;
^††Laboratório de Abelhas Nativas, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Campus Universitário, Trindade, 88.040-900 Florianópolis, Brazil;
^‡‡Centro de Investigaciones Biológicas, Facultad de Humanidades, Universidad del Zulia, Apartado Postal 526, Maracaibo 4011, Zulia, Venezuela; and
^§§Division of Biology, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, United Kingdom

Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved February 29, 2008 (received for review October 31, 2007)

Abstract

Water reservoirs formed by the leaf axils of bromeliads are a highly derived system for nutrient and water capture that also house a diverse fauna of invertebrate specialists. Here we investigate the origin and specificity of bromeliad-associated insects using Copelatinae diving beetles (Dytiscidae). This group is widely distributed in small water bodies throughout tropical forests, but a subset of species encountered in bromeliad tanks is strictly specialized to this habitat. An extensive molecular phylogenetic analysis of Neotropical Copelatinae places these bromeliadicolous species in at least three clades nested within other Copelatus. One lineage is morphologically distinct, and its origin was estimated to reach back to 12–23 million years ago, comparable to the age of the tank habitat itself. Species of this clade in the Atlantic rainforest of southern Brazil and mountain ranges of northern Venezuela and Trinidad show marked phylogeographical structure with up to 8% mtDNA divergence, possibly indicating allopatric speciation. The other two invasions of bromeliad water tanks are more recent, and haplotype distributions within species are best explained by recent expansion into newly formed habitat. Hence, bromeliad tanks create a second stratum of aquatic freshwater habitat independent of that on the ground but affected by parallel processes of species and population diversification at various temporal scales, possibly reflecting the paleoclimatic history of neotropical forests.

Footnotes

^‡To whom correspondence should be sent at the present address:
Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543.
E-mail: michael_balke{at}yahoo.de
Author contributions: M.B., J.G.-Z., and A.P.V. designed research; M.B., J.G.-Z., I.R., A.V., A.Z., J.S., M.G., and L.H. performed research; M.B. and J.G.-Z. analyzed data; and M.B., J.G.-Z., I.R., and A.P.V. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database [accession nos. AM947384–AM947434 (cob), AM945966–AM946014 (rrnL), AM945593–AM945649 (cox1), and AM945690–AM945739 (h3)].
This article contains supporting information online at www.pnas.org/cgi/content/full/0710368105/DCSupplemental.