Evolutionary process of deep-sea bathymodiolus mussels

Abstract

Background: Since the discovery of deep-sea chemosynthesis-based communities, much work has been done to clarify their organismal and environmental aspects. However, major topics remain to be resolved, including when and how organisms invade and adapt to deep-sea environments; whether strategies for invasion and adaptation are shared by different taxa or unique to each taxon; how organisms extend their distribution and diversity; and how they become isolated to speciate in continuous waters. Deep-sea mussels are one of the dominant organisms in chemosynthesis-based communities, thus investigations of their origin and evolution contribute to resolving questions about life in those communities.

Methodology/principal finding: We investigated worldwide phylogenetic relationships of deep-sea Bathymodiolus mussels and their mytilid relatives by analyzing nucleotide sequences of the mitochondrial cytochrome c oxidase subunit I (COI) and NADH dehydrogenase subunit 4 (ND4) genes. Phylogenetic analysis of the concatenated sequence data showed that mussels of the subfamily Bathymodiolinae from vents and seeps were divided into four groups, and that mussels of the subfamily Modiolinae from sunken wood and whale carcasses assumed the outgroup position and shallow-water modioline mussels were positioned more distantly to the bathymodioline mussels. We provisionally hypothesized the evolutionary history of Bathymodilolus mussels by estimating evolutionary time under a relaxed molecular clock model. Diversification of bathymodioline mussels was initiated in the early Miocene, and subsequently diversification of the groups occurred in the early to middle Miocene.

Conclusions/significance: The phylogenetic relationships support the "Evolutionary stepping stone hypothesis," in which mytilid ancestors exploited sunken wood and whale carcasses in their progressive adaptation to deep-sea environments. This hypothesis is also supported by the evolutionary transition of symbiosis in that nutritional adaptation to the deep sea proceeded from extracellular to intracellular symbiotic states in whale carcasses. The estimated evolutionary time suggests that the mytilid ancestors were able to exploit whales during adaptation to the deep sea.

Figure 1. The sampling sites for deep-sea Bathymodiolus mussels and their relatives used in this study.

Refer to Table 2 for details of the sampling sites. ○, hydrothermal vent; •, cold-water seep; ▪, wood/whale bone; ▴, shallow.

Figure 2. The sampling sites for deep-sea Bathymodiolus mussels and their relatives in Japanese waters.

The boxed region in Fig. 1 is enlarged. Refer to Table 2 for details of the sampling sites. ○, hydrothermal vent; •, cold-water seep; ▪, wood/whale bone; ▴, shallow.

Figure 3. Phylogenetic relationships of deep-sea Bathymodiolus mussels and their relatives based on the 401-bp COI and 423-bp ND4 sequences.

The NJ tree was constructed based on the genetic distances calculated according to Kimura's two-parameter method using Modiolus nipponicus as an outgroup species. The MP and Bayesian trees presented essentially the same topology as the NJ tree. Only the NJ (left) and MP (middle) bootstrap values >50% and Bayesian posterior probabilities (right) >0.50 are specified. The scale bar indicates 0.01 substitutions per site. See Table 1 for abbreviations of Bathymodiolus mussels and their relatives. ○, hydrothermal vent; •, cold-water seep; ▪, wood/whale bone; ▴, shallow.

Figure 4. Posterior distribution of evolutionary divergence times.

Phylogenetic relationships of deep-sea Bathymodiolus mussels based the concatenated 401-bp COI and 423-bp ND4 sequences. The ML tree was constructed using Modiolus nipponicus as an outgroup species. The red lines represent 95% credibility intervals of sampled values. See Table 2 for abbreviations of Bathymodiolus mussels.

Figure 5. Schematic representation of evolutionary symbiostic transition.

Mytilid mussels from shallow water with no symbionts; Benthomodiolus geikotsucola from whale carcasses haboring extracellular symbionts trapped by microvilli of the host cells; Adipicola pacifica from whale carcasses haboring extracellular symbionts enclosed by the protrudent host cell membrane; A. crypta from whale carcasses haboring intracellular symbionts; Bathymodiolus mussels with intracellular symbionts.