Genomic evidence for facultative selfing in the cichlid fish Cyphotilapia frontosa

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Abstract

Organisms have evolved a remarkable diversity of reproductive strategies in response to environmental variations and selective pressures. Although most vertebrates do reproduce biparentally, rare alternative modes such as selfing (self-fertilization) and different forms of parthenogenesis exist, but remain poorly characterized. Here, we investigated an unusual reproductive event in the normally biparental cichlid fish Cyphotilapia frontosa , in which a female produced offspring in the absence of a male. Using whole-genome sequencing data, we analyzed whether reproduction occurred via selfing or parthenogenesis by comparing patterns of heterozygosity with those from a wild, genetically diverse C. frontosa family collected in Lake Tanganyika and a closely related inbred Ctenochromis benthicola family. The uniparental family exhibited reduced genetic diversity, elevated relatedness, and genome-wide patterns of homozygosity distinct from those expected under parthenogenesis or inbreeding, but consistent with self-fertilization. Our study provides rare genomic evidence of selfing in a vertebrate and suggests that such alternative reproductive modes may be overlooked rather than truly absent. These findings contribute to a broader understanding of how alternative reproductive strategies evolve in vertebrate lineages. Significance The overwhelming majority of vertebrates reproduce sexually, requiring a male and a female to produce genetically distinct offspring. Yet, rare alternative modes involving only a single parent such as asexual parthenogenesis (“virgin birth”) or self-fertilization challenge this paradigm. Among these, selfing is exceptionally uncommon and poorly studied in vertebrates. Here, we unveiled - based on genomic analyses - the reproductive strategy of a member of the extraordinarily diverse cichlid fish radiation in Lake Tanganyika that reproduced in captivity in the absence of a male. By comparing patterns of genome-wide heterozygosity with both wild and inbred reference families, we identified a rare case of selfing. This finding adds to the limited records of selfing in vertebrates and expands current understanding of reproductive diversity, highlighting the power of whole-genome sequencing to distinguish among alternative reproductive mechanisms.
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Abstract Organisms have evolved a remarkable diversity of reproductive strategies in response to environmental variations and selective pressures. Although most vertebrates do reproduce biparentally, rare alternative modes such as selfing (self-fertilization) and different forms of parthenogenesis exist, but remain poorly characterized. Here, we investigated an unusual reproductive event in the normally biparental cichlid fish Cyphotilapia frontosa, in which a female produced offspring in the absence of a male. Using whole-genome sequencing data, we analyzed whether reproduction occurred via selfing or parthenogenesis by comparing patterns of heterozygosity with those from a wild, genetically diverse C. frontosa family collected in Lake Tanganyika and a closely related inbred Ctenochromis benthicola family. The uniparental family exhibited reduced genetic diversity, elevated relatedness, and genome-wide patterns of homozygosity distinct from those expected under parthenogenesis or inbreeding, but consistent with self-fertilization. Our study provides rare genomic evidence of selfing in a vertebrate and suggests that such alternative reproductive modes may be overlooked rather than truly absent. These findings contribute to a broader understanding of how alternative reproductive strategies evolve in vertebrate lineages. Significance The overwhelming majority of vertebrates reproduce sexually, requiring a male and a female to produce genetically distinct offspring. Yet, rare alternative modes involving only a single parent such as asexual parthenogenesis (“virgin birth”) or self-fertilization challenge this paradigm. Among these, selfing is exceptionally uncommon and poorly studied in vertebrates. Here, we unveiled - based on genomic analyses - the reproductive strategy of a member of the extraordinarily diverse cichlid fish radiation in Lake Tanganyika that reproduced in captivity in the absence of a male. By comparing patterns of genome-wide heterozygosity with both wild and inbred reference families, we identified a rare case of selfing. This finding adds to the limited records of selfing in vertebrates and expands current understanding of reproductive diversity, highlighting the power of whole-genome sequencing to distinguish among alternative reproductive mechanisms. Competing Interest Statement The authors have declared no competing interest.

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License: CC-BY-NC-4.0