Genetic connectivity in US Caribbean queen conch (Aliger gigas):Implications for management and forensic assignment

Abstract

Understanding genetic connectivity among marine populations is central to conservation biology, informing how exploited species are managed, and how marine protected area (MPA) networks are designed. The queen conch (Aliger gigas) is a large, heavily exploited Caribbean gastropod listed under CITES Appendix II and provides an ideal system for examining connectivity in species with high dispersal potential. Its extended pelagic larval phase promotes gene flow across broad spatial scales, limiting detectable population structure. Here we used low-coverage whole-genome sequencing (lcWGS) of queen conch sampled from three regions within United States waters, Florida (FL), Puerto Rico (PR), and the US Virgin Islands (VI), to characterize connectivity and to evaluate the implications for management. Using genotype-likelihood approaches, we inferred patterns across principal component analysis, admixture analysis, pairwise FST, contemporary migration, and historical coalescent-based demographic modeling. Genome-wide analyses revealed little structure with individuals from all three regions intermixed in ordination space and similar ancestry profiles, consistent with high gene flow. In contrast, analyses restricted to the upper tail of the FST distribution recovered geographically concordant structure, resolving FL, PR, and VI as distinguishable groups, with PR individuals showing intermediate, admixed ancestry between FL and VI. Estimates of contemporary migration indicated a partially open system in which 72-98% of each population's ancestry was locally derived, with substantial bidirectional gene flow between PR and VI, moderate immigration from VI into FL and VI to PR, and negligible direct exchange from FL to either PR or VI. Historical demographic analyses suggest long-term genetic effective population sizes (Ne) on the order of 2.2-7.6 x 105; individuals and a hierarchical population divergence during the early Pleistocene (~ 2 Mya) with ongoing symmetric migration among the three populations, with the strongest historical connectivity between PR and VI with 10 diploid migrants per generation (2Nm = 20.0). Together, these results indicate that queen conch populations across US waters are neither fully panmictic nor completely isolated. Instead, they form a connected population system in which substantial gene flow occurs alongside geographically differentiated genomic variation. These findings argue against treating the US range as either a single management unit or as a set of completely independent stocks. They also highlight the potential importance of the US Virgin Islands within the regional connectivity network and suggest that highly differentiated loci could be useful for developing forensic SNP panels to identify the geographic origin of queen conch products and support enforcement against illegal, unreported, and unregulated fishing.