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Open Access Highly Accessed Research article

Evolution of microgastropods (Ellobioidea, Carychiidae): integrating taxonomic, phylogenetic and evolutionary hypotheses

Alexander M Weigand1*, Adrienne Jochum1, Rajko Slapnik2, Jan Schnitzler13, Eugenia Zarza13 and Annette Klussmann-Kolb13

Author Affiliations

1 Department of Phylogeny and Systematics, Institute for Ecology, Evolution and Diversity, Biosciences, Goethe-University Frankfurt, Max-von-Laue Straße 13, 60438, Frankfurt am Main, Germany

2 Institute of Biology, Center for Scientific Research of the Slovenian Academy of Sciences and Arts, Novi trg 2, p.p. 306, 1000, Ljubljana, Slovenia

3 Biodiversity and Climate Research Centre, Senckenberganlage 25, 60325, Frankfurt am Main, Germany

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BMC Evolutionary Biology 2013, 13:18  doi:10.1186/1471-2148-13-18

Published: 23 January 2013

Abstract

Background

Current biodiversity patterns are considered largely the result of past climatic and tectonic changes. In an integrative approach, we combine taxonomic and phylogenetic hypotheses to analyze temporal and geographic diversification of epigean (Carychium) and subterranean (Zospeum) evolutionary lineages in Carychiidae (Eupulmonata, Ellobioidea). We explicitly test three hypotheses: 1) morphospecies encompass unrecognized evolutionary lineages, 2) limited dispersal results in a close genetic relationship of geographical proximally distributed taxa and 3) major climatic and tectonic events had an impact on lineage diversification within Carychiidae.

Results

Initial morphospecies assignments were investigated by different molecular delimitation approaches (threshold, ABGD, GMYC and SP). Despite a conservative delimitation strategy, carychiid morphospecies comprise a great number of unrecognized evolutionary lineages. We attribute this phenomenon to historic underestimation of morphological stasis and phenotypic variability amongst lineages. The first molecular phylogenetic hypothesis for the Carychiidae (based on COI, 16S and H3) reveals Carychium and Zospeum to be reciprocally monophyletic. Geographical proximally distributed lineages are often closely related. The temporal diversification of Carychiidae is best described by a constant rate model of diversification. The evolution of Carychiidae is characterized by relatively few (long distance) colonization events. We find support for an Asian origin of Carychium. Zospeum may have arrived in Europe before extant members of Carychium. Distantly related Carychium clades inhabit a wide spectrum of the available bioclimatic niche and demonstrate considerable niche overlap.

Conclusions

Carychiid taxonomy is in dire need of revision. An inferred wide distribution and variable phenotype suggest underestimated diversity in Zospeum. Several Carychium morphospecies are results of past taxonomic lumping. By collecting populations at their type locality, molecular investigations are able to link historic morphospecies assignments to their respective evolutionary lineage. We propose that rare founder populations initially colonized a continent or cave system. Subsequent passive dispersal into adjacent areas led to in situ pan-continental or mountain range diversifications. Major environmental changes did not influence carychiid diversification. However, certain molecular delimitation methods indicated a recent decrease in diversification rate. We attribute this decrease to protracted speciation.

Keywords:
Integrative taxonomy; Protracted speciation; Subterranean environment; Cryptic diversity; DNA barcoding; Allopatric diversification; Carychium; Zospeum; Phylogeny; Gastropoda