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PreprintCited by 10Genetic and Clinical Aspects of Sex Determination and Chromosomal AbnormalitiesReproductive biology and impacts on aquatic speciesChromosomal and Genetic Variations

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Mitonuclear sex determination? Empirical evidence from bivalves

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Smith, Chase H., Mejia-Trujillo, Raquel, Breton, Sophie, Pinto, Brendan J., Kirkpatrick, Mark, Havird, Justin C.·2023·Molecular Biology and Evolution
DOI 10.1101/2023.07.05.547839PMC PMC10653589

Preprint — published as 10.1093/molbev/msad240 · Paper page

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Abstract

Genetic elements encoded in nuclear DNA determine the sex of an individual in many animals. In bivalves, however, mitochondrial DNA (mtDNA) has been hypothesized to contribute to sex determination in lineages that possess doubly uniparental inheritance (DUI). In these cases, females transmit a female mtDNA (F mtDNA) to all offspring, while male mtDNA (M mtDNA) is transmitted only from fathers to sons. Because M mtDNA is inherited in the same way as Y chromosomes, it has been hypothesized that mtDNA may be responsible for sex determination. However, the role of mitochondrial and nuclear genes in sex determination has yet to be validated in DUI bivalves. In this study, we used DNA, RNA, and mitochondrial short non-coding RNA (sncRNA) sequencing to explore the role of mitochondrial and nuclear elements in the sexual development pathway of the freshwater mussel Potamilus streckersoni (Bivalvia: Unionida). We found that the M mtDNA shed a sncRNA partially within a male-specific mitochondrial gene that targeted pathways hypothesized to be involved in female development and mitophagy. RNA-seq confirmed the gene target was significantly upregulated in females, supporting a direct role of mitochondrial sncRNAs in gene silencing. These findings support the hypothesis that M mtDNA inhibits female development. Genome-wide patterns of genetic differentiation and heterozygosity did not support a nuclear sex determining region, although we cannot reject that nuclear factors are involved with sex determination. Our results provide further evidence that mitochondrial loci contribute to diverse, non-respiratory functions and provide a first glimpse into an unorthodox sex determining system.

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Metadata

Authors
Smith, C. H., Mejia-Trujillo, R., Breton, S., Pinto, B. J., Kirkpatrick, M., & Havird, J. C.
Affiliations
  • The University of Texas at Austin (US)
  • Université de Montréal (CA)
  • Milwaukee Public Museum (US)
Corresponding author
Smith, Chase H.
ORCID
Venue
Molecular Biology and Evolution
Publisher
openRxiv
Published
2023-07-07
Volume
40
Issue
11
ISSN
0737-4038 (ISSN-L)
DOI
10.1101/2023.07.05.547839
PMC
PMC10653589
OpenAlex
W4388448188
Cited by
10
References
1
Citations by year
2026: 1 · 2025: 4 · 2024: 5
FWCI
1.83
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Molecular Biology and Evolution (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nd)
Funders
  • University of Texas at Austin (SCR_021713)
  • National Institutes of Health (SCR_021713)
  • National Institute of General Medical Sciences (R35GM142836)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
Keywords
doubly uniparental inheritance, mitochondrial DNA, gene silencing, mitophagy, female development, freshwater mussels, Unionida, sexual development, heterozygosity, genetic differentiation

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