Abstract
Female sperm storage (FSS) has been reported in Chondrichthyans species, and involves the prolonged maintenance of viable sperm after mating events, prior to egg fertilization. Along with multiple paternity (MP–female producing offspring of multiple males within the same litter), FSS has been hypothesized to be related to the increased reproductive fitness of cartilaginous fish lineages. The present study aimed to investigate if: (1) are FSS and MP evolutionarily related and share the same evolutionary history in Chondrichthyes? (2) How is the presence of FSS implied by extinction and speciation rates and thus related to the current species diversity of the group? To answer these questions, we obtained FSS and MP records for Chondrichthyes species from the literature and performed ancestral reconstruction analyses for each character in the phylogenetic tree. We employed MEDUSA and MiSSE to determine if the shifts in diversification rates were related to the characters along the phylogeny. Finally, we utilized HiSSE to calculate the net diversity rates for observed and unobserved states. The ancestral reconstruction indicates that both characters are plesiomorphic for the group; FSS is suggested to be absent in Lamniformes and Rhinopristiformes, whereas MP may be absent in Galeocerdo cuvier. MEDUSA and MiSSE revealed that all clades lacking FSS showed no increase in rates, while there was a higher diversification rates in clades with FSS. HiSSE identified lower net diversity rates in clades lacking FSS associated with hidden states. Therefore, FSS absence seems to contribute to increased extinction rates by reducing diversity among the Chondrichthyes.
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Acknowledgements
The authors would like to thank the Ichthyology Laboratory (UFRGS) team for their help in developing this study and Flavia Petean, Karla Soares and Renan Maestri for corrections and suggestions on earlier versions of the manuscript. We would also like to thank CAPES, CNPq and FAPERGS for the research grants and scholarships.
Funding
The authors were financially supported by the Brazilian Coordination for the Improvement of Higher Education Personnel (CAPES) (88887.600666/2021–00), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Produtividade em Pesquisa (313834/2021-0ALN-F), and the Fundação de Amparo à Pesquisa no Rio Grande do Sul (FAPERGS) ARD/ARC(72550.751.48979 ALN-F).
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Felipe Lamarca collected the data, performed the analyses, prepared all the figures and wrote the main manuscript text. Pedro Hollanda Carvalho and André Luiz Netto-Ferreira designed and directed this study. All the authors reviewed and approved the manuscript.
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10682_2024_10305_MOESM1_ESM.xlsx
Reports on occurrence of female sperm storage and multiple paternity in Chondrichthyes species. The following information is in the table, families with the number of total species described in parentheses accord to Eschmeyer's Catalog of Fishes (Fricke 2024), number of total samples investigated and the number of samples with the occurrence of the characters confirmed in each study, and * for studies that confirmed the presence of FSS, but did not report the number of samples analyzed for each species or the number of samples with confirmed occurrence. (XLSX 19 kb)
10682_2024_10305_MOESM2_ESM.xlsx
Complete result of female sperm storage character-dependent diversification estimates in the HiSSE framework and the character-independent diversification estimates in the MiSSE framework. (XLSX 16 kb)
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Lamarca, F., Carvalho, P.H. & Netto-Ferreira, A.L. The loss of female sperm storage ability as a potential driver for increased extinction in Chondrichthyes. Evol Ecol (2024). https://doi.org/10.1007/s10682-024-10305-4
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DOI: https://doi.org/10.1007/s10682-024-10305-4