Cryptic Barriers to Gene Flow Driven by Deep-Sea Reproductive Strategy in Direct-Developing Pandalid Shrimp

Some deep-sea crustaceans produce larger eggs, which are hypothesised to be an adaptation to the food-scarce deep-sea environment, promoting development of larger offspring with enhanced starvation resistance. Larger offspring also adhere more strongly to benthic substrates, reducing the risk of being advected by currents. Limited dispersal likely increases genetic differentiation among regional populations. Pandalus coccinatus and its putative sister species, Pandalus spinosior, are cold-water pandalid shrimps that live at depths of 400-500 m along the Pacific and Okhotsk coasts of Japan, respectively. Unlike other marine species, P. coccinatus and P. spinosior develop directly without a pelagic larval stage and produce a small number of large eggs, making them ideal models for investigating the relationship between reproductive strategy and genetic patterns in deep-sea crustaceans. In this study, we collected 24-30 specimens from each of three locations across the species range and investigated genetic differentiation among populations. We used mitochondrial DNA (mtDNA) cytochrome c oxidase subunit I (COI) gene sequences and multiplexed inter-simple sequence repeat genotyping, employing MIG-seq, which provides genome-wide single-nucleotide polymorphisms (SNPs). We also examined diagnostic morphological traits and assessed congruence between morphological taxonomy and genetic patterns revealed by molecular markers. Our findings present a conceptual framework in which deep-sea adaptations lead to reduced larval dispersal, increased genetic differentiation, and allopatric speciation, accompanied by morphological divergence. This study suggests that benthic deep-sea animals may undergo significant diversification as a result of both adaptive traits and environmental barriers, potentially explaining the unexpectedly high levels of biodiversity in deep-sea benthic communities.