Recombination in the eggs and sperm in a simultaneously hermaphroditic vertebrate

Author:

Theodosiou L.1,McMillan W. O.2,Puebla O.342ORCID

Affiliation:

1. Max-Planck-Institute for Evolutionary Biology, Research Group for Community Dynamics, August-Thienemann-Straße 2, 24306 Plön, Germany

2. Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Panamá, República de Panamá

3. GEOMAR Helmholtz Centre for Ocean Research Kiel, Evolutionary Ecology of Marine Fishes, Düsternbrooker Weg 20, 24105 Kiel, Germany

4. Faculty of Mathematics and Natural Sciences, University of Kiel, Christian-Albrechts-Platz 4, 24118 Kiel, Germany

Abstract

When there is no recombination (achiasmy) in one sex, it is in the heterogametic one. This observation is so consistent that it constitutes one of the few patterns in biology that may be regarded as a ‘rule’ and Haldane (Haldane 1922 J. Genet. 12 , 101–109. ( doi:10.1007/BF02983075 )) proposed that it might be driven by selection against recombination in the sex chromosomes. Yet differences in recombination rates between the sexes (heterochiasmy) have also been reported in hermaphroditic species that lack sex chromosomes. In plants—the vast majority of which are hermaphroditic—selection at the haploid stage has been proposed to drive heterochiasmy. Yet few data are available for hermaphroditic animals, and barely any for hermaphroditic vertebrates. Here, we leverage reciprocal crosses between two black hamlets ( Hypoplectrus nigricans , Serranidae), simultaneously hermaphroditic reef fishes from the wider Caribbean, to generate high-density egg- and sperm-specific linkage maps for each parent. We find globally higher recombination rates in the eggs, with dramatically pronounced heterochiasmy at the chromosome peripheries. We suggest that this pattern may be due to female meiotic drive, and that this process may be an important source of heterochiasmy in animals. We also identify a large non-recombining region that may play a role in speciation and local adaptation in Hypoplectrus .

Funder

Smithsonian Competitive Grants Program for Science

DFG

Smithsonian Tropical Research Institute Short-Term Fellowship

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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