Comparative phylogeography of the ocean planet

Abstract

Understanding how geography, oceanography, and climate have ultimately shaped marine biodiversity requires aligning the distributions of genetic diversity across multiple taxa. Here, we examine phylogeographic partitions in the sea against a backdrop of biogeographic provinces defined by taxonomy, endemism, and species composition. The taxonomic identities used to define biogeographic provinces are routinely accompanied by diagnostic genetic differences between sister species, indicating interspecific concordance between biogeography and phylogeography. In cases 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. Here, we provide examples of comparative phylogeography from (i) tropical seas that host the highest marine biodiversity, (ii) temperate seas with high productivity but volatile coastlines, (iii) migratory marine fauna, and (iv) plankton that are the most abundant eukaryotes on earth. Tropical and temperate zones both show impacts of glacial cycles, the former primarily through changing sea levels, and the latter through coastal habitat disruption. The general concordance between biogeography and phylogeography indicates that the population-level genetic divergences observed between provinces are a starting point for macroevolutionary divergences between species. However, isolation between provinces does not account for all marine biodiversity; the remainder arises through alternative pathways, such as ecological speciation and parapatric (semiisolated) divergences within provinces and biodiversity hotspots.

Keywords: biogeography; coral reefs; evolution; marine biodiversity; speciation.

Fig. 1.

(A) Biogeographic provinces of the tropical Indo-Pacific as defined by >10% endemism (18). Coral triangle is indicated in dark blue. Primary barriers include (site I) Red Sea Barrier, (site II) Indo-Pacific Barrier, and (site III) East Pacific Barrier. (B–E) Minimaps illustrating widespread species with phylogeographic separation (strong allele-frequency shifts and significant F-statistics) at peripheral provinces. For each panel, the peripheral region(s) of phylogeographic distinction is highlighted in color, and photos are of the species with genetic evidence for that pattern as follows: (B) Hawai’i and the Red Sea [1, Mulloidichthys flavolineatus (19); 2, Corallochaetodon species complex (20); 3, Panulirus penicillatus (21); 4, Chaetodon auriga (22)]; (C) Red Sea only [5, Pygoplites diacanthus (23); 6, Neoniphon sammara (24)]; (D) Hawai’i only [7, Pristipomoides filamentosus (25); 8, Chaetodon ornatissimus (26); 9, Acanthurus nigroris (27)]; (E) Marquesas/French Polynesia [10, Parupeneus multifasciatus (28); 11, Acanthurus nigrofuscus (29); 12, Lutjanus fulvus (30); 13, Lutjanus kasmira (30)]. Photo credits: J. E. Randall/FishBase (photograph 7); Tane Sinclair-Taylor (all other fish photographs); Matthew Iacchei (photograph of Panulirus penicillatus).

Fig. 2.

Evidence of isolation across the Indo-Pacific Barrier. (A) Distribution patterns of sister species pairs. Distributions shaded in purple (and indicated by arrows) represent areas of species overlap. (B) Phylogeographic studies demonstrating divergent genetic lineages within species. Black and white in pie diagrams indicate distribution of mtDNA phylogroups separated by at least three mutations. In all cases, there is evidence of population expansion with overlap in the Indo Malay-Philippine biodiversity hotspot (Coral Triangle) (47). Myripristis berndti data from Craig et al. (48), Cephalopholis argus data from Gaither et al. (49), Sphyrna lewini data from Duncan et al. (50), and Nerita albicilla data from Crandall et al. (51). COI, cytochrome oxidase subunit 1; Cyt b, cytochrome b. Photo credit: J. E. Randall for fishes, Wikimedia commons/Harry Rose for Nerita albicilla.

Fig. 3.

Sardines (genus Sardinops) and Anchovies (genus Engraulis) are antitropical species that recently surmounted the warm-water barrier between northern and southern hemispheres, as indicated by mtDNA haplotype networks. For sardines in the East Pacific, transequatorial dispersal is facilitated by a short and steep continental shelf and adjacent deep cold water (78). For anchovies in the East Atlantic, transequatorial dispersal is facilitated by upwelling (cold nutrient-rich water) in low latitudes (107). Light and dark haplotypes indicate northern and southern hemisphere, respectively. Squares connected by a dashed line indicate haplotypes shared between hemispheres. Note that, in the East Pacific sardine, the haplotype shared between northern and southern hemisphere is internal to both networks, indicating an ancient connection. In contrast, the East Atlantic anchovy has connections across the equator that include both interior and peripheral haplotypes in the network.