Range-wide genetic erosion signal and deep population divergence in the declining mud shrimp Upogebia pugettensis

Abstract

The Blue Mud Shrimp, Upogebia pugettensis , is an ecosystem engineer of western North American estuaries and strongly influences estuarine biogeochemical cycling, surface area, biodiversity, and trophic dynamics. In recent decades, U. pugettensis populations have declined or been extirpated over the species’ range due to infestations by the introduced Asian isopod parasite Orthione griffenis . These widespread losses highlight a need for a conservation strategy. The genetic structure of U. pugettensis populations is a critical metric for such conservation efforts but had not been previously characterized. We therefore surveyed U. pugettensis populations from California to Alaska to assess patterns of genetic diversity and differentiation, including isolation by distance and potential barriers to gene flow using the RADseq approach. We found moderate overall genetic diversity but extremely low observed heterozygosity and consistently high inbreeding coefficients across populations, especially in Alaska. Pairwise F ST values, Principal Component Analysis (PCA), TESS ancestry models, and AMOVA analysis revealed a pronounced north-south genetic break, with additional substructure among southern populations. The widespread heterozygote deficit is likely to have resulted from recent demographic bottlenecks that, in turn, may have been driven by O. griffenis induced host castration and reproductive collapses. Given the severity of infestations, the presence of the resistant congener Upogebia major , and limited prospects for natural recovery, we recommend urgent conservation actions for the most impacted U . pugettensis populations. Our findings highlight the vulnerability of estuarine invertebrates to compounding anthropogenic threats and emphasize the need for proactive management in the face of accelerating environmental change.

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