Genetically based resistance to summer mortality in the Pacific oyster (Crassostrea gigas) and its relationship with physiological, immunological characteristics and infection processes
Introduction
According to Koganezawa (1974), the phenomenon known as Crassostrea gigas “summer mortality” first began along the Japanese Pacific coast in 1945. Features common to mortality episodes were elevated temperature, full maturation or spawning and high trophic conditions. The relationship between gonadal maturation, energy metabolism, and the mortalities was investigated (Koganezawa, 1974, Mori, 1979) and it was concluded that summer mortality in Japan was due to a “physiological disorder and metabolic disturbance derived by heavy gonad formation and massive spawning under high water temperature and eutrophication” (Koganezawa, 1974). In the late 1950s, mortalities of C. gigas were first noted on the west coast of USA (Glude, 1975, Cheney et al., 2000). Experimental studies further implicated gonadal maturation and loss of carbohydrate reserves (Perdue et al., 1981). Lipovsky and Chew (1972) showed experimentally that rising temperature (up to 21 °C) or high levels of microalgae significantly increased mortality. Different pathogens were isolated but none of them could explain summer mortality (Elston et al., 1987, Friedman et al., 1998, Friedman et al., 1991, Friedman et al., 2005). In France, oyster production has experienced periodical mass mortalities for the last 20 years (Renault et al., 1994, Goulletquer et al., 1998, Soletchnik et al., 1999). Results have confirmed that summer mortality is the result of multiple factors including elevated temperature, physiological stress associated with maturation, aquaculture practices, pathogens, pollutants, etc… (Soletchnik et al., 1997, Soletchnik et al., 2006, Goulletquer et al., 1998, Le Roux et al., 2002, Le Roux, 2004, Gay et al., 2004a). Despite inter-annual and inter-livestock variability, mortality of oysters reared on the sediment (or a few centimetres above) was significantly higher (20–30%) than mortality of animals on tables (iron frames) (Soletchnik et al., 1999, Soletchnik et al., 2003, Soletchnik et al., 2005). The Morest project on C. gigas oyster summer mortality (2001–2005) progressively classified the importance of these different factors by coupling field and experimental studies (Samain et al., 2004a, Samain et al., 2004b, Soletchnik et al., 2005). Summer mortality has also been described in cultured eastern oysters, C. virginica, on the north-eastern coasts of the USA where a disease named Juvenile Oyster Disease (JOD) was reported. This disease only affects juvenile (< 1 year old) and fast growing oysters when seawater temperature exceeds 20 °C and plankton blooms occur (Lee et al., 1996). JOD can cause the death of up to 90% of affected stocks within a few weeks (Bricelj et al., 1992, Ford and Borrero, 2001). Studies have shown a genetic basis for the resistance to JOD allowing the production of resistant strains (Lewis et al., 1996).
Increasing stress and disease tolerance of economically important species has long been considered feasible through selective breeding. For oysters, genetic variability is thought to be a major determinant in sensitivity to summer mortality (Hershberger et al., 1984). Selected families produced in a breeding program showed greatly improved survival both in the field and in elevated temperature laboratory trials (Beattie et al., 1980). However these selected stocks appeared thinner, smaller and had slower growth than unselected stocks. During the Morest project, Dégremont et al. (2005) showed that 45% of the observed variance in mortality in the field was due to variation among families. Such resistance, against a complex of factors affecting survival, is a very attractive model for understanding biological resistance mechanisms. Moreover, natural populations are likely to be under selective pressure and consequently eliminate susceptible oysters. However, these observations suggest a possible difference in fitness and adaptation between resistant and susceptible oysters in different environments. In this paper, we describe the results of divergent selection based on these criteria, and present a review of the main biological aspects associated with resistance or susceptibility, by comparison of field and experimental data from different disciplines.
Section snippets
Biological material
A first generation (G1), constituted of 44 full-sib families and 17 half-sib families, was produced following a hierarchical mating design in 2001 as described by Dégremont et al. (2005). Oysters were deployed and tested until October 2001 in Rivière d'Auray located in South Brittany in France (2°57′W 47°36′N). According to their mean survival performances, 3 half-sib families (each constituted of 3 full-sib families) showing high survival and 3 showing high mortality were selected. In a second
R and S mortality, growth and yield
Mortality, individual weight (initial and final) and yield are presented in Table 2. The R group showed much higher survival than the S group and the control group had intermediate survival (p < 0.0001) for both generations in Rivière d'Auray (i.e., G2 and G3 from 2002 and 2003 respectively). For example in 2002 for G2, summer mortality of the S oysters was 43%, while it was only 7% for R oysters and 24% for the unselected control. Similar results were found in 2003 for G3 where summer mortality
Genetic effect
R oysters demonstrated a better survival than S oysters indicating a positive response to selection for survival. These findings, combined with similar growth observed for the two selected groups and the unselected control, gave an overall higher yield for R compared with S, and intermediate yield in the control. Landgon et al. (2003) reported that yield is a heritable trait, but without distinguishing the relative influence of survival and growth. In Rivière d'Auray, survival explains most of
Conclusion
A difference in the reproductive status of R and S oysters appeared to be a key factor in the differential response to infection. But even if the energy decrease associated with reproduction intensity and temperature plays a role in summer mortality, the measured differences in reproduction intensity and in related respiration rates were quite small. These could not explain phenotypic differences between R and S except if other events, such as stress or spawning events, accentuate the energetic
Acknowledgments
The authors are grateful to all the contributors involved in the Morest project for their support during the course of this work. We are indebted to H. McCombie-Boudry for her help with English language editing. We thank L. Dégremont for providing the parental oysters and all the staff of Argenton (especially P. Le Souchu, J.P. Connan and I. Quéau) and Bouin (especially M. Nourry) stations for providing experimental oysters under controlled conditions. We also thank all the staff of La
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