Testing dispersal limits in the sea: range‐wide phylogeography of the pronghorn spiny lobster Panulirus penicillatus

Abstract

Aim To resolve phylogeographical partitions in the pronghorn spiny lobster, Panulirus penicillatus, which has a nine-month pelagic larval phase and the broadest distribution among spiny lobsters. With samples from the Red Sea to the East Pacific, we test genetic partitions across two-thirds of the planet, in a species with one of the longest pelagic phases.Location Red Sea, Indian and Pacific Oceans.Methods A fragment of the mtDNA cytochrome c oxidase subunit I gene (COI) was resolved in 774 individuals from 28 locations, plus 55 sequences (10 locations) from public databases. Portions of COI, 12S and 16S mtDNA regions were resolved for phylogenetic analyses on a subset of individuals. Phylogenetic and population-level analyses were used to detect evolutionary partitions and dispersal barriers.Results Significant population structuring was detected (overall Φ ST = 0.310, P < 0.001). Samples from the Red Sea and East Pacific Provinces (western and eastern range edges) comprise distinct phylogenetic lineages, divergent at d = 1.1% and 1.8%, respectively, from the Indo-Pacific. Coalescent analyses indicate a Pleistocene isolation for the Red Sea (0.71 Ma) and East Pacific (1.52 Ma). Excluding the Red Sea and East Pacific, structure across the rest of the range was comparatively low, but significant (Φ ST = 0.018, P < 0.001).Main conclusions The Red Sea and East Pacific populations are phylogenetically distinct from populations elsewhere in the range. The East Pacific population diverged earliest, and may represent a distinct subspecies. Phylogeographical divisions align with the major Indo-Pacific biogeographical barriers, and with subsets of provincial designations from two frameworks: one based on levels of endemism and one on species composition. Tropical and temperate regions in the Pacific are significantly differentiated, potentially indicating an ecological partition. Isolation at eastern and western peripheral provinces may serve as a starting point for evolutionary diversification within this group.

Comparative phylogeography of the ocean planet

“…The pronghorn spiny lobster, Panulirus penicillatus, with a 9-mo pelagic larval duration and a distribution across the entire tropical Indo-Pacific, illustrates genetic diversification at both ends of its range. Iacchei et al (21) found fixed differences in mtDNA of East Pacific and Red Sea populations (Φ ST = 0.74), corroborated by morphological differentiation in the East Pacific (58). Speciation in peripheral provinces is apparent in Thalassoma wrasses (59), Anampses wrasses (60), Acanthurus surgeonfishes (55), Mulloidichthys goatfishes (19), and Montastraea corals (61).…”

“…The East Pacific Barrier (EPB) limits the distribution of tropical species (62), with few taxa able to maintain population connectivity across the EPB, as evidenced by the lobster P. penicillatus (21), and the coral Porites lobata (63,64). However, some fishes (65) and the echinoderm Echinothrix diadema (66) have low or insignificant Φ ST values across the EPB.…”

“…For example, Hawaiian limpets of the genus Cellana have diversified within the archipelago along a tidal gradient that indicates ecological speciation (104). Certainly, species sharing population structure at unexpected locations within biogeographic provinces (such as Fiji in the tropical Pacific) (21,105), or other exceptions to those general trends, will provide evolutionary insights.…”

Seascape genetics of the spiny lobster Panulirus homarus in the Western Indian Ocean: Understanding how oceanographic features shape the genetic structure of species with high larval dispersal potential

“…Where individual species are distributed across two or more biogeographic provinces, shifts in genotype frequencies often align with biogeographic boundaries, providing intraspecific concordance between biogeography and phylogeography. Recent examples among marine taxa include sea snails (Brante, Fernández, & Viard, ); clams (DeBoer et al., ); Indo‐Pacific goatfish, Mulloidichthys flavolineatus (Fernandez‐Silva et al, ); spiny lobster, Panulirus penicillatus (Iacchei, Gaither, Bowen, & Toonen, ); barnacles (Ewers‐Saucedo et al, ); and seaweeds in the southeast Pacific (Guillemin et al, ).…”

Introduction to virtual issue on Red Sea and Western Indian Ocean biogeography

“…() examine a widespread goatfish species and find that phylogeographical breaks are congruent with existing boundaries of biogeographical provinces, and that these peripheral biogeographical provinces may represent evolutionary incubators for reef fishes ( sensu Bowen et al., ). Broadening the taxonomic scope, Iacchei, Gaither, Bowen and Toonen () find similar concordance of phylogeographical and biogeographical barriers in the spiny lobster (also see Bowen et al., ). Higher‐resolution studies such as Priest et al.…”