A genomic test of sex- biased dispersal in white sharks

• 成果类型: Article
• 署名作者: Laso-Jadart, Romuald; Corrigan, Shannon L.; Yang, Lei; Lee, Szu- Hsuan; Gay, Elise J.; Fedrigo, Olivier; Lowe, Christopher G.; Skomal, Gregory; Cliff, Geremy; Padilla, Mauricio Hoyos; Huveneers, Charlie; Lyons, Kady; Sato, Keiichi; Glancy, James; Lesturgie, Pierre; Mona, Stefano; Naylor, Gavin J. P.
• 署名单位: Universite PSL; Ecole Pratique des Hautes Etudes (EPHE); Sorbonne Universite; Universite PSL; Ecole Pratique des Hautes Etudes (EPHE); Rockefeller University; California State University System; California State University Long Beach; University of Massachusetts System; University of Kwazulu Natal; Flinders University South Australia; British Museum of Natural History
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-13316
• DOI: 10.1073/pnas.2507931122
• 发表日期: 2025-08-12
• 关键词: carcharodon-carcharias; population-structure; reproductive philopatry; genetic-structure; reef sharks; r-package; mitochondrial; nuclear; FRAMEWORK; inference

摘要

Mitonuclear discordance has been observed in several shark species. Female philopatry has often been invoked to explain such discordance but has never been explicitly tested. Here, we focus on the white shark, for which female philopatry has been previously proposed, and produced a chromosome-level genome, high-coverage whole-genome autosomal, and uniparental datasets to investigate mitonuclear discordance. We first reconstructed the historical population demography of the species based on autosomal data. We show that this species once comprised a single panmictic population, which experienced a steady decline until recent times when it fragmented into at least three main autosomal genetic groups. Mitochondrial data depict a strikingly different picture, inconsistent with the spatial distribution of autosomal diversity. Using the demographic scenario established from autosomal data, we performed coalescent and forward simulations to test for the occurrence of female philopatry. Coalescent simulations showed that the model can reproduce the autosomal variability, confirming its robustness. A forward simulation framework was further built to explicitly account for a sex-biased reproduction model and track both autosomal and uniparental markers (Y chromosome and mitochondrial DNA). While our model generates data that are consistent with the observed Y chromosome variation, the mitochondrial pattern is never reproduced even under extreme female philopatry (no female migration), strongly suggesting that demography alone cannot explain the mitonuclear discordance. Our framework could, and perhaps should, be extended to other shark species where philopatry has been suggested. It is possible that the proposed widespread occurrence of female philopatry in sharks should be revisited. Significance The mitonuclear discordance seen in sharks is widely attributed to female philopatry but has never been explicitly tested. Herein, we explore the issue in white sharks, for which we assembled a high-resolution genome and reconstructed the demographic history using resequencing data. We used backward and forward simulations to examine the genetic consequences of sex-specific migration patterns using parameter values derived from the demographic analyses of autosomal data. The mitochondrial variability observed in natural populations was never reproduced in any of the simulations-even under extreme female philopatry, suggesting that other forces have contributed to the discordance. The same approach would benefit other species of shark where female philopatry has previously been assumed based on genetic data.