Genetic Diversity and Phylogeography of a Turf-Forming Cosmopolitan Marine Alga, Gelidium crinale (Gelidiales, Rhodo-Phyta)

Abstract

Cosmopolitan species are rare in red algae, which have a low-dispersal capacity unless they are dispersed by human-mediated introductions. Gelidium crinale, a turf-forming red alga, has a widespread distribution in tropical and temperate waters. To decipher the genetic diversity and phylogeography of G. crinale, we analyzed mitochondrial COI-5P and plastid rbcL sequences from collections in the Atlantic, Indian, and Pacific Oceans. Phylogenies of both markers statistically supported the monophyly of G. crinale, with a close relationship to G. americanum and G. calidum from the Western Atlantic. Based on the molecular analysis from these materials, Pterocladia heteroplatos from India is here merged with G. crinale. Phylogeny and TCS networks of COI-5P haplotypes revealed a geographic structure of five groups: (i) Atlantic-Mediterranean, (ii) Ionian, (iii) Asian, (iv) Adriatic-Ionian, and (v) Australasia-India-Tanzania-Easter Island. The most common ancestor of G. crinale likely diverged during the Pleistocene. The Bayesian Skyline Plots suggested the pre-LGM population expansion. Based on geographical structure, lineage-specific private haplotypes, the absence of shared haplotypes between lineages, and AMOVA, we propose that the cosmopolitan distribution of G. crinale has been shaped by Pleistocene relicts. The survival of the turf species under environmental stresses is briefly discussed.

Keywords: Gelidium crinale; Pleistocene relict; biogeography; cosmopolitan distribution; geographical structure; red algae.

Figure 1

Maximum likelihood (ML) phylogeny (A) and split network (B) of Gelidium crinale using 33 unique mitochondrial COI-5P sequences. ML bootstrap values (≥50%) and Bayesian posterior probabilities (≥0.9) are shown at branches. Dash indicates values <50 or <0.9.

Figure 2

TCS-derived network and geographic distribution of 33 haplotypes of G. crinale based on mitochondrial COI-5P. (A) Haplotype network. Each circle denotes a single haplotype with size proportional to frequency. Small open circles represent missing haplotypes. Haplotypes are colored according to the country as shown in the key. Haplogroup follows phylogroups in Figure 1 and Figure S1. (B) Distribution map of haplotypes. Pie charts denote the proportion of haplotypes present in each location. Private and shared haplotypes are colored as shown in the key.

Figure 3

Mismatch distribution analysis (MDA) and Bayesian skyline plot (BSP) of Gelidium crinale using a mitochondrial COI-5P dataset. (A) MDA of overall species; (B) MDA of group I; (C) MDA of group III; (D) MDA of the Western Atlantic realm; (E) BSP of overall species; (F) BSP of group I; (G) BSP of group III; (H) BSP of the Western Atlantic realm. For mismatch distributions, the grey bar charts represent the observed distributions, whereas the black lines represent simulated data under a sudden expansion model. For BSPs, the x-axis represents the time since the present in years and the y-axis represents the estimated effective population size (N_e). Light blue color indicates BSP for Group I, red for Group III, and pink for the Western Atlantic. The solid center line is the median estimate, and the upper and lower lines indicate the 95% highest posterior density (HPD) intervals for N_e.

Figure 4

Type specimens of P. heteroplatos analyzed in this study. (A): Holotype specimen (Børgesen 5275 in C); (B): Isotype specimen (PC 0452740, labelled as ‘cotype’).

Figure 5

Habit (A–D) of representative specimens and map (E) of collection sites of Gelidium crinale. (A): France; (B): England; (C): Vietnam; (D): Korea. Color dots indicate six biogeographic realms (blue, Eastern Atlantic; purple, Western Atlantic; red, Asia; orange, Western Indo-Pacific; green, Temperate Australasia; yellow, Eastern Indo-Pacific).