The ocean is not deep enough: pressure tolerances during early ontogeny of the blue mussel Mytilus edulis

Abstract

Early ontogenetic adaptations reflect the evolutionary history of a species. To understand the evolution of the deep-sea fauna and its adaptation to high pressure, it is important to know the effects of pressure on their shallow-water relatives. In this study we analyse the temperature and pressure tolerances of early life-history stages of the shallow-water species Mytilus edulis. This species expresses a close phylogenetic relationship with hydrothermal-vent mussels of the subfamily Bathymodiolinae. Tolerances to pressure and temperature are defined in terms of fertilization success and embryo developmental rates in laboratory-based experiments. In M. edulis, successful fertilization under pressure is possible up to 500 atm (50.66 MPa), at 10, 15 and 20 degrees C. A slower embryonic development is observed with decreasing temperature and with increasing pressure; principally, pressure narrows the physiological tolerance window in different ontogenetic stages of M. edulis, and slows down metabolism. This study provides important clues on possible evolutionary pathways of hydrothermal vent and cold-seep bivalve species and their shallow-water relatives. Evolution and speciation patterns of species derive mostly from their ability to adapt to variable environmental conditions, within environmental constraints, which promote morphological and genetic variability, often differently for each life-history stage. The present results support the view that a direct colonization of deep-water hydrothermal vent environments by a cold eurythermal shallow-water ancestor is indeed a possible scenario for the Mytilinae, challenging previous hypothesis of a wood/bone to seep/vent colonization pathway.

Figure 1

Schematic of the experimental pressure vessels: (a) plastic vial filled with the egg suspension and the microcentrifuge tube half-filled with sperm suspension; (b) pressure vessel showing the plastic vials inside (arrow indicates the connection valve to the hydraulic pump).

Figure 2

Mytilus edulis embryonic and early larval development incubated at different pressure/temperature regimes for 50 hours, with fertilization occurring at atmospheric pressure. Histograms are of percentage mean and standard deviation. Stages of development: A=abnormal; 0=unfertilized; I=fertilized, uncleaved egg; II=two-cell; III=four-cell; IV=eight-cell; V=multi-cell; VI=early blastula; VII=gastrula; VIII=early trochophore; IX=late trochophore; X=D-larva (see table 1 for a detailed description of each developmental stage).

Figure 3

Mytilus edulis embryonic development incubated at different pressure/temperature regimes for 4 hours, with fertilization occurring under pressure. Histograms are of percentage mean and standard deviation. Stages of development: A=abnormal; 0=unfertilized; I=fertilized, uncleaved egg; II=two-cell; III=four-cell; IV=eight-cell; V=multi-cell (see table 1 for a detailed description of each developmental stage).

Figure 4

Mytilus edulis embryonic and early larval development incubated at different pressure/temperature regimes for 24 hours, with fertilization occurring under pressure. Histograms are of percentage mean and standard deviation. Stages of development: A=abnormal; 0=unfertilized; I=fertilized, uncleaved egg; II=two-cell; III=four-cell; IV=eight-cell; V=multi-cell; VI=early blastula; VII=gastrula; VIII=early trochophore; IX=late trochophore; X=D-larva (see table 1 for a detailed description of each developmental stage).