Genetic and morphological divergences in the cosmopolitan deep-sea amphipod Eurythenes gryllus reveal a diverse abyss and a bipolar species

Abstract

Eurythenes gryllus is one of the most widespread amphipod species, occurring in every ocean with a depth range covering the bathyal, abyssal and hadal zones. Previous studies, however, indicated the existence of several genetically and morphologically divergent lineages, questioning the assumption of its cosmopolitan and eurybathic distribution. For the first time, its genetic diversity was explored at the global scale (Arctic, Atlantic, Pacific and Southern oceans) by analyzing nuclear (28S rDNA) and mitochondrial (COI, 16S rDNA) sequence data using various species delimitation methods in a phylogeographic context. Nine putative species-level clades were identified within E. gryllus. A clear distinction was observed between samples collected at bathyal versus abyssal depths, with a genetic break occurring around 3,000 m. Two bathyal and two abyssal lineages showed a widespread distribution, while five other abyssal lineages each seemed to be restricted to a single ocean basin. The observed higher diversity in the abyss compared to the bathyal zone stands in contrast to the depth-differentiation hypothesis. Our results indicate that, despite the more uniform environment of the abyss and its presumed lack of obvious isolating barriers, abyssal populations might be more likely to show population differentiation and undergo speciation events than previously assumed. Potential factors influencing species' origins and distributions, such as hydrostatic pressure, are discussed. In addition, morphological findings coincided with the molecular clades. Of all specimens available for examination, those of the bipolar bathyal clade seemed the most similar to the 'true' E. gryllus. We present the first molecular evidence for a bipolar distribution in a macro-benthic deep-sea organism.

Figure 1. Sample localities of Eurythenes gryllus sensu lato.

Abbreviations refer to samples from this study, that of France and Kocher and Escobar-Briones et al. (for details see Table 1). The sampling region in the Southern Ocean is shown as an enlargement. Color codes are provided for each sampling locality and are used consistently in the other figures.

Figure 2. Tree constructions on the three-gene dataset.

Bayesian (BI) and Maximum Parsimony (MP) trees inferred for specimens of Eurythenes gryllus sampled in this study, based on the combined dataset of three genes (COI, 16S rDNA, 28S rDNA), showing posterior probabilities (>0.5) and bootstrap values (>50%; number of bootstrap replicates = 2,000), respectively. Two bootstrap values are shown at each node, the upper one represents the value when gaps were treated as fifth characters whilst the lower one represents the value when gaps were treated as missing data. The different clusters are assigned with the codes Eg1–5. For each cluster, distributional ranges (ocean basin, bathyal vs. abyssal, depth) are indicated. The colored squares refer to the sample localities of Figure 1.

Figure 3. Bayesian tree inferred for the 16S rDNA dataset of Eurythenes gryllus.

Posterior probabilities (>0.5) are shown at each node. In the case of identical sequences, all specimens are listed with corresponding abbreviations. For the sequences retrieved from GenBank , , the accession number of the haplotype as well as the number of specimens per haplotype is indicated (when higher than 1). The different clusters are assigned with the codes Eg1–9. For each cluster, distributional ranges (ocean basin, bathyal vs. abyssal, depth) are indicated.

Figure 4. Statistical parsimony haplotype networks based on the 16S rDNA sequences of Eurythenes gryllus.

The dataset includes sequences from this study, that of France and Kocher and Escobar-Briones et al. . The area of each circle is proportional to the frequency of the haplotype in our sampling (a scale is presented). Each line represents a single substitution, nodes represent hypothetical haplotypes and colors refer to the sampling localities. Haplotype networks (95% probability threshold) are numbered (Eg1–9) according to the different clusters identified in Figures 2–3.

Figure 5. Major morphological differences observed between Eurythenes clades.

Numbers (1–15) refer to the numbers of the characters presented in Table 4. Illustrated specimens have either been sequenced (*) or belong to genetically and morphologically homogeneous samples, of which some specimens have been sequenced and the best preserved specimens have been illustrated (**). (1) A, specimen BraB-8* from Eg6; B, specimen ArgB-7* from Eg3, (2)(3) A, specimen KGI** from Eg1; B–C, specimen ArgB-7* from Eg3, (4) A, specimen BraB-8* from Eg6; B, specimen ArgB-7* from Eg3, (5) A, specimen KGI** from Eg1; B, specimen ArgB-7* from Eg3, (6) A, specimen KGI** from Eg1; B, specimen ArgB-7* from Eg3, (7) A, specimen KGI** from Eg1; B, specimen ArgB-7* from Eg3, (8)(9) A, specimen KGI** from Eg1; B, specimen ArgB-7* from Eg3, (10)(11)(12) A, specimen BraB-8* from Eg6; B, specimen ArgB-7* from Eg3, (13) A, specimen Ant-a1* (juvenile) from Eg2; B, specimen ArgB-4* (juvenile) from Eg3, (14)(15) A, specimen Ant-a1* (juvenile) from Eg2; B, specimen ArgB-4* (juvenile) from Eg3.