The case of Dermo disease

1. Simulation of the development of disease resistance in oyster populations using a gene-based population dynamics model The case of Dermo disease Eric Powell, Eileen Hofmann, John Klinck, Ximing Guo, Susan Ford, Dave Bushek, and others

2. Why does Perkinsus marinus persist as a major source of mortality in oyster populations? The challenge of developing disease resistance for the eastern oyster Crassostrea virginica

3. Adult Mortality -- 1953-2009 Delaware Bay oysters become completely MSX resistant Dermo Era MSX Era Partial MSX disease resistance develops

4. The Delaware Bay Scenario: the Dermo era High-mortality epizootics 1 & 2 level High-mortality epizootic 3 level Medium-mortality epizootic level Low-mortality level

5. The Goal Investigation of the development of disease resistance in naïve populations newly challenged with disease! Can the response of the population be modeled such that the future trajectory of genetic response can be inculcated into long-term restoration strategy?

6. The Challenge: Implementation of a gene-based population dynamics model DyPoGEn (Dynamic Population Genetics Engine), a model designed to simulate population dynamics from the genotype through the phenotype to the population

7. G3 G1 }L1 }L2 G2 G4 Model Configuration 10 Chromosome pairs 4 Genes per chromosome 2 Alleles per gene (A, B) Sex gene identifying protandric animals and permanent males Genetic subroutines Meiosis Crossing-over Random chromosome sorting at reproduction Determination of phenotype from genotype

8. G3 G1 }L1 }L2 G2 G4 Model Configuration Larval subroutine Larval survivorship as a function of post-settlement abundance (compensatory broodstock-recruitment) Adult subroutine • Age • Growth at age • Sex change at size • Determination of parent pairs • Reproduction at size • Mortality at age

9. G3 G1 }L1 }L2 G2 G4 Model Configuration 14 Loci with disease-resistant alleles 12 show dominance 2 show underdominance Distributions: C1-1 C2-1 C3-1 C4-2 C7-3 C8-2 C9-3 C10-1 A allele resistant; B allele sensitive Naïve population A allele frequency 10% Naïve population B allele frequency 90% Whole animal fitness: 14 AA loci; fitness=1 Whole animal fitness: 14 BB loci; fitness~0

10. Imposed Levels of Epizootic Mortality Gulf Coast representative rate : Level 4 = 40% Delaware Bay representative rates: Level 3 = 25% Level 2 = 22% Limited disease challenge rate: Level 1 = 17% Naïve rate: Level 0 = 13% Onset of Dermo disease Challenged population Unchallenged population

11. Impact of Disease Challenge:Population Abundance Declines Population Average Age Declines

12. The Genetic Response to Disease Challenge: Population Average Fitness Increases Fitness of naïve population: average = 0.1 on a 0-to-1 scale Fitness increases over time in challenged population

13. Example Set of Fitness Trajectories Key modulators of outcome to disease challenge: 1. Increased mortality increases the rate of disease resistance BUT 2. Selection versus drift: drift can limit the ambit of response through allele loss Impact of drift at high mortality Onset of disease challenge

14. Outcome of Selection at 22% Epizootic Mortality A range in population dynamics affects the outcome very little. Only the presence of a few controlling alleles permits a much higher level of disease resistance. Overall, disease resistance develops, but at a very slow rate. Significant change in disease resistance occurs on half-century time scale

15. Outcome of Selection at 40% Epizootic Mortality A range in population dynamics affects the outcome considerably. Population dynamics minimizing drift result in significant increases in disease resistance over 10-20 years. Fewer controlling alleles, however, permit nearly complete disease resistance in 10-20 years. Reduced genetic determination High growth, increased fecundity, high abundance

16. The Manager’s Dilemma A total mortality rate of 15-25% per year produces population decline. An epizootic mortality rate of 25% per year limits fishing to de minimis rates. A total mortality rate of 15-25% per year limits development of disease resistance to half-century or longer time scales. Era of overfishing Dermo era reference pt. based de minimis fishery 40% rule reference pt. MSX partially resistant population

17. The Delaware Bay Scenario High-mortality epizootics 1 & 2 level Lower high-mortality level: epizootic 3 ~15 years post-onset Medium-mortality epizootic level Low-mortality level

18. Conclusions • Dermo disease resistance develops slowly due to the number of alleles involved. • Time scales are multi-decadal unless total mortality rate is high (e.g., 40%). • Slow rate of disease resistance development in Delaware Bay suggests many alleles are involved and, thus, disease resistance will continue to develop at increasingly slower rates. • Epizootic mortality rates that fail to support rapid disease resistance nevertheless result in significant reductions in abundance and curtailment of anything but a de minimis fishery. • No manipulation of population dynamics through restoration or recruitment enhancement will encourage further development of disease resistance, although it may support a higher level of abundance.