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Island isolation reduces genetic diversity and connectivity but does not significantly elevate diploid male production in a neotropical orchid bee

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Abstract

There is concern about the worldwide decline of bees, in which genetic factors may play a role. As populations of these haplodiploid insects suffer habitat fragmentation and subsequent isolation, theory predicts an increase in inbreeding and a concomitant increase in inviable or sterile diploid males, a product of reduced allelic diversity at the sex determining locus, which could lead to a diploid male extinction vortex. To test this idea, we genotyped 1,245 males of one orchid bee, Euglossa cordata, a species with low diploid male production on the mainland. We genotyped bees from the Brazilian mainland and three islands using five highly variable microsatellite loci. Allelic richness was lowest on the most remote island 38 km from the mainland and, though the degree of differentiation across localities was modest (global FST = 0.034; global \({\text{G}}_{\text{ST}}^{'} = 0. 1 5 3\), both P < 0.001) and isolation by distance was weak (Mantel test, r = 0.614, P = 0.056), sea was revealed to be a significant barrier to inferred historic gene flow (partial Mantel test of distance over sea, r = 0.831, P = 0.003). Only seven males were diploid (mean diploid male production, DMP, 0.6 %). Though the proportion of diploid males was highest on the most remote island (1.3 %), differences in DMP across study areas were statistically non-significant. Thus island isolation leads to reduced genetic variation at putatively neutral microsatellite loci, but E. cordata nevertheless seems to maintain allelic diversity at the sex locus, possibly because of sufficient gene flow, or because it is a locus under balancing selection, or because of the joint action of these two evolutionary forces: migration and selection. These and other bee species may be able to maintain sufficient variability at the sex locus to avoid entering the DM extinction vortex, even on relatively isolated islands or habitat fragments.

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Acknowledgments

We thank Carlos Eduardo Pinto, Guaraci Duran Cordeiro, Morgana Sazan, Paulo César Fernandes and Tiago Caetano for their help in the field, André Nemésio and Leo Rocha Filho for species identification, Flávio Oliveira Francisco, Leandro Rodrigues Santiago, Paulo Gonçalves and Rita Radzeviciute for help in the lab, and Maria Cristina Arias, Tomás Murray and the referees for many very helpful comments that helped improve the manuscript. Petra Liebe kindly processed samples in a MegaBace in the Molecular Ecology Lab at the Martin Luther University Halle-Wittenberg, for which we thank her and Robin Moritz. The Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) supported our project. The Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the Deutscher Akademischer Austausch Dienst (DAAD) funded the first author. SISBIO (Sistema de Informação e Autorização em Biodiversidade) provided a collecting permit (Nr.10453-1) and IBAMA (Insituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis) provided a biological sample export permit (Nr.10BR005548/DF).

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  1. Departamento de Biologia, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Av. Bandeirantes, 3900, Bloco 2, Ribeirão Prêto, SP, 14040-901, Brazil

    Samuel Boff

  2. General Zoology, Institute for Biology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 8, 06120, Halle (Saale), Germany

    Samuel Boff, Antonella Soro & Robert J. Paxton

  3. German Centre for Integrative Biodiversity Research (iDiv), Halle-Jena-Leipzig, Deutscher Platz 5e, 04103, Leipzig, Germany

    Robert J. Paxton

  4. Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 321, trav 14. Cidade Universitária, São Paulo, SP, 05508-900, Brazil

    Isabel Alves-dos-Santos

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  1. Samuel Boff
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Correspondence to Samuel Boff.

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Boff, S., Soro, A., Paxton, R.J. et al. Island isolation reduces genetic diversity and connectivity but does not significantly elevate diploid male production in a neotropical orchid bee. Conserv Genet 15, 1123–1135 (2014). https://doi.org/10.1007/s10592-014-0605-0

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