Coupled biophysical global ocean model and molecular genetic analyses identify multiple introductions of cryptogenic species

Abstract

The anthropogenic introduction of exotic species is one of the greatest modern threats to marine biodiversity. Yet exotic species introductions remain difficult to predict and are easily misunderstood because knowledge of natural dispersal patterns, species diversity, and biogeography is often insufficient to distinguish between a broadly dispersed natural population and an exotic one. Here we compare a global molecular phylogeny of a representative marine meroplanktonic taxon, the moon-jellyfish Aurelia, with natural dispersion patterns predicted by a global biophysical ocean model. Despite assumed high dispersal ability, the phylogeny reveals many cryptic species and predominantly regional structure with one notable exception: the globally distributed Aurelia sp.1, which, molecular data suggest, may occasionally traverse the Pacific unaided. This possibility is refuted by the ocean model, which shows much more limited dispersion and patterns of distribution broadly consistent with modern biogeographic zones, thus identifying multiple introductions worldwide of this cryptogenic species. This approach also supports existing evidence that (i) the occurrence in Hawaii of Aurelia sp. 4 and other native Indo-West Pacific species with similar life histories is most likely due to anthropogenic translocation, and (ii) there may be a route for rare natural colonization of northeast North America by the European marine snail Littorina littorea, whose status as endemic or exotic is unclear.

Fig. 1.

Molecular phylogeny of Aurelia reveals many cryptic species with predominantly limited geographic distributions. Shown are maximum likelihood nrDNA (–Ln = 7425) and COI (–Ln = 4725) gene trees. Bootstrap values of >50% are shown above (maximum likelihood, 1,000 realizations, excluding gapped positions in nrDNA) or below (unweighted maximum parsimony, 10,000 realizations, including gapped positions in nrDNA) each branch. (Scale bars represent 0.025 substitutions per site.) Trees were rooted with sequences from Cyanea spp. (and also Phacellophora COI). *, calculated excluding outgroup taxa; support for other nodes increased 3–10% over values shown or remained at 100%.

Fig. 2.

Network of the most parsimonious relationship between the 20 COI haplotypes sequenced from Aurelia sp. 1. Each circle represents a different haplotype; the area of each circle or segment is proportional to the frequency with which that haplotype was observed (largest to smallest circles: 30, 12, 6, 5, 3, 2, 1). The color of each segment indicates the geographic origin of that fraction of the samples. Each branch of unit length represents a 1-nucleotide mutation. Small squares indicate a haplotype that does, or did, exist but that we did not sample. Genetic diversity (mean ± SD) is high in Japan (h = 0.87 ± 0.06; π = 0.0063 ± 0.0037; n = 26) and low elsewhere (California: h = 0.53 ± 0.14; π = 0.0020 ± 0.0015; n = 16; Australia: h = 0.66 ± 0.08; π = 0.0048 ± 0.0029; n = 37). In subsequent analyses, eastern and western Australia (EA and WA) are treated as one unit due to the small WA sample (n = 6), because all WA haplotypes are found in EA so there is no significant difference between regions (Φ_ST = 0; P = 0.97) and because ocean modeling indicates that EA and WA may be well connected on evolutionary time scales (Fig. 3). Most California sequences taken from ref. were cloned, whereas new sequences for this study were direct sequenced. Consequently, in contrast to other unique haplotypes, the three unique California haplotypes may result from PCR error made unambiguous by sequencing cloned amplicons.

Fig. 3.

Final year CODs (colored marine areas and scale) for releases in the five primary zones of occurrence of Aurelia sp.1 (adjacent red land areas, east Australia release; Inset, west Australia release). The COD around Japan is derived from a 10,000-year simulation, and the others are derived from 1,000-year simulations; all have reached a quasistable state. Black and red contours represent estimated maximum extent of particles based on samples taken over the integration period for open and closed North Atlantic boundary, respectively. COD is the sum over all time steps of the number of particles in a particular grid box for the lifespan (1 year) of the particles. Gray shading (see scale bar) indicates the proportional effect of temperature on survivorship of medusae before reproduction and can be interpreted as an index of establishment probability or reproductive viability of a population, integrated over the medusa and polyp phases, consistent with evidence of temperature effects in Aurelia (24) and with species introductions that occur predominantly along lines of similar latitude (45). Symbols show the distribution of known phylogenetic species of Aurelia based on COI and nrDNA (circles), 16S and partial-nrDNA (squares), or COI (triangle) sequence data (see Table 2). Species are numbered as in Fig. 1, or represented by a letter code: A, Aurelia aurita; B, Aurelia labiata; CA, Cyanea-Aurelia hybrid (39); M, Aurelia limbata; R, Aurelia“ARAB” (39). An additional nrDNA haplotype, “mca,” of unknown geographic origin has been documented (39) (see Table 2 and Fig. 10).

Fig. 4.

Final year COD for initial releases of Aurelia sp.4 from Borneo and the Philippines, i.e., within the region in which Aurelia sp.4 is endemic. Contours, shading, and symbols are as described in Fig. 3, although the temperature indices for survivorship of Aurelia sp. 4 (T_max = 36°C and T_min = 23°C) are markedly different to sp. 1, favoring tropical conditions.