The little shrimp that could: phylogeography of the circumtropical Stenopus hispidus (Crustacea: Decapoda), reveals divergent Atlantic and Pacific lineages.

‘Ale‘Alani Dudoit,William E Browne,Michelle R Gaither,Brian W Bowen,Richard R Coleman,Matthew Iacchei,Robert J Toonen

doi:10.7717/peerj.4409

‘Ale‘Alani Dudoit, William E Browne + Show 5 more

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https://doi.org/10.7717/peerj.4409

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Abstract

The banded coral shrimp, Stenopus hispidus (Crustacea: Decapoda: Stenopodidea) is a popular marine ornamental species with a circumtropical distribution. The planktonic larval stage lasts ∼120–253 days, indicating considerable dispersal potential, but few studies have investigated genetic connectivity on a global scale in marine invertebrates. To resolve patterns of divergence and phylogeography of S. hispidus, we surveyed 525 bp of mitochondrial cytochrome c oxidase subunit I (COI) from 198 individuals sampled at 10 locations across ∼27,000 km of the species range. Phylogenetic analyses reveal that S. hispidus has a Western Atlantic lineage and a widely distributed Indo-Pacific lineage, separated by sequence divergence of 2.1%. Genetic diversity is much higher in the Western Atlantic (h = 0.929; π = 0.004) relative to the Indo-Pacific (h = 0.105; π < 0.001), and coalescent analyses indicate that the Indo-Pacific population expanded more recently (95% HPD (highest posterior density) = 60,000–400,000 yr) than the Western Atlantic population (95% HPD = 300,000–760,000 yr). Divergence of the Western Atlantic and Pacific lineages is estimated at 710,000–1.8 million years ago, which does not readily align with commonly implicated colonization events between the ocean basins. The estimated age of populations contradicts the prevailing dispersal route for tropical marine biodiversity (Indo-Pacific to Atlantic) with the oldest and most diverse population in the Atlantic, and a recent population expansion with a single common haplotype shared throughout the vast Indian and Pacific oceans. In contrast to the circumtropical fishes, this diminutive reef shrimp challenges our understanding of conventional dispersal capabilities of marine species.

Highlights

Despite the seemingly broad continuity of the world’s oceans, relatively few marine species achieve and maintain circumtropical distributions
Phylogenetic analyses revealed two lineages that corresponded to a Western Atlantic lineage observed at Curacao, Belize, and Panama and an Indo-Pacific lineage consisting of all sample sites in the Pacific Ocean, Red Sea and Indian Ocean (Bayesian posterior probability = 1.0; ML bootstrap = 93; NJ = 95) (Fig. 2)
The high genetic structure and reciprocal monophyly together indicate a prolonged period with no gene flow between these ocean basins, and this inference is further supported by our to most recent common ancestor (TMRCA) dates (Fig. 2)

Summary

Introduction

Despite the seemingly broad continuity of the world’s oceans, relatively few marine species achieve and maintain circumtropical distributions. In a recent survey of fishes, Gaither et al (2015a) found that fewer than 1% have circumtropical distributions. Seventy percent of these cosmopolitan fishes are species that thrive in the relatively continuous, and comparatively environmentally stable habitat of the bathypelagic zone (>200 m depth). Many other circumtropical fishes are large pelagic species, such as billfishes, sharks, and tunas, with adult ranges spanning whole ocean basins and broad depth distributions (Castro et al, 2007; Collette et al, 2011). No parallel synthesis has been conducted for invertebrates, and the few examples of circumtropical invertebrates we found in the literature were either pelagic or mesopelagic species (e.g., Norris, 2000; Van der Spoel & Heyman, 1983), associated with open ocean currents (e.g., Trickey, Thiel & Waters, 2016; Willan, 1979), or fouling organisms of cryptogenic origin (e.g., Foster & Willan, 1979; Jones, 1992)

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