Pinpointing the level of isolation between two cryptic species sharing the same microhabitat: a case study with a scarabaeid species complex

Authors: ROY, LISE - University Of Montpellier; BON, MARIE-CLAUDE - European Biological Control Laboratory (EBCL); CESARINI, CYRIL - University Of Montpellier; SERIN, JOSE - Csiro European Laboratory; BONATO, OLIVIER - Institute For Research And Development In Agri-Environment(IRDA)

Submitted to: Zoologica Scripta
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/12/2015
Publication Date: 7/1/2016
Citation: Roy, L., Bon, M., Cesarini, C., Serin, J., Bonato, O. 2016. Pinpointing the level of isolation between two cryptic species sharing the same microhabitat: a case study with a scarabaeid species complex. Zoologica Scripta. 45(4):407-420.

Interpretive Summary: In 2009, the Commonwealth Scientific and Industrial Research Organization (CSIRO) decided to introduce an exotic dung beetle, Onthophagus vacca L. into south-east Australia, aiming at reducing the problems associated with the accumulation of dung from 30 million cattle and 200 million sheep. In 2010, an importation permit was issued by the Australian Quarantine and Inspection Service (AQIS) for importing O. vacca from Southern France to Australia. However during the same year, a taxonomic revision circumscribed the O. vacca species to the lighter form and ranked the melanic form to another species O. medius, thereby restricting the importation to one form only, presupposing that pure populations of the lighter form exist in southern France. The purpose of the present study was to better characterize the two species and determine the level of isolation between the two by integrating morphological analysis, genetic analysis, and intra and interspecific mating and crossing bioassays. All findings concur with the conclusion that the two species are reproductively isolated, and clearly pinpoint allopatric O. vacca s.s. populations in Languedoc Roussillon (Southern of France) for exportation to Australia in compliance with the ongoing permit. This study supports the utility of integrative taxonomy approaches to delineate species and shows that where there is doubt about species status in this case. In order to avoid possible errors, validation by genetic and phenotypic analysis should be required for import permit applications. Integrative approach as described in this paper has resulted in the accelerated introduction into Australia of an important dung beetle species.

Technical Abstract: We explored biological processes underlying speciation within dung beetles belonging to the vacca species complex (Scarabaeidae: Onthophagus). The two taxa of this complex, O. vacca and O. medius, not only are known to have a large overlapping Palearctic distribution range but also share the same cowpat with no physical barriers and no observed specific aggregated patterns in the local distribution. The present study aimed at determining the level of isolation between the two taxa and discussed the most likely scenario of the speciation (sympatry vs. allopatry). We conducted a full study on populations sampled within the Mediterranean region integrating morphological analysis (digital image analysis of the elytral melanism pattern), two-gene phylogenies, population genetic analyses on populations sampled from an area where both species occur and another one with O. vacca only, as well as intra- and interspecific mating and crossing bioassays. The variation in the elytral melanism pattern clearly followed a bimodal distribution, with O. medius being more melanic than O. vacca, with a very limited overlapping area. The two taxa are reproductively isolated, with a strong postzygotic incompatibility despite the absence of sexual isolation. Sequence analysis of both nuclear and mitochondrial markers revealed a deep divergence between the two taxa dating back to 8.7 Mya. All findings concurred with some phenological observations and the conclusion that the most likely scenario for speciation in the vacca complex was an allopatric speciation followed by secondary contact.