Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Harvest-induced life-history evolution in exploited fish populations Bruno Ernande Laboratoire Ressources Halieutiques IFREMER Boulogne-sur-Mer, France Empirical evidence and forecasting of evolutionary changes and their demographic consequences

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Fishing as a global issue ∎ More than 80% of fish stocks are fully or overexploited ∎ World captures have reached a ceiling since the late 80’s FAO.2010.SOIA report

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Fisheries-induced selection and expected adaptive changes ∎ Fisheries-induced selection: fishing mortality is 4 to 5 times higher than natural mortality ∎ Life history traits are primarily under selection Age and size at maturation: Fish that reproduce too late are fished before they can do so. Reproductive effort: Investing into future reproduction is not useful when there is none. Growth rate: Small fish that stay below mesh size for longer may have more offspring during their lifetime. ∎ Adaptive changes in life history traits may imply both Fisheries-induced phenotypically plasticity Fisheries-induced adaptive evolution (adaptive genetic change) ∎ Nonadaptive changes in life history traits may arise from Fisheries-induced neutral evolution

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Issues at stake ∎ Changes in life history traits affect stocks’ demography Fisheries production Population viability  Sustainable exploitation and restoration of the stocks (Johannesburg 2002) ∎ The nature of processes is of primary importance for management purposes Plastics changes are reversed on a within-generation timescale Evolutionary changes on a between-generation timescale (decades).  Fisheries Common Policy (EU) ∎ Biodiversity Changes in life history traits  functional diversity Changes in genetic composition  genetic diversity  Reduction of the alteration of biodiversity (Green Paper EU 2001; Johannesburg 2002)

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Outline 1.Empirical evidence: the nature of adaptive processes 2.Evolutionary equilibria expected under fishing-induced selection and demographic implications Deterministic cohort-based model of phenotypic evolution 3.Harvest-induced evolutionary rates and potential mitigation measures Deterministic cohort-based model of quantitative genetic evolution (coupled with dynamic optimization) 4.Fisheries-induced adaptive vs. neutral evolution and effects on genetic diversity Stochastic individual-based model of genetic evolution

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April Empirical evidence: The nature of adaptive processes

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Northern cod case study: background information Olsen et al. (2004) Nature Continuous decline since the 70’s Année A50 (année) A50 : age at which 50% of the fish are mature

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 ∎ Compensatory response (phenotypic plasticity): Decreased biomass > Increased growth > Earlier maturation and/or ∎ Evolution of age and size at maturation (genetic modification): Size-selective fishing favors genotypes characterized by early maturation at small size Two hypotheses Olsen et al. (2004) Nature

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 BaselineCompensatory response (fast growth) Age size Growth trajectories Reaction norm Maturation reaction norm (MRN) analysis: Principle EvolutionCompensatory response and evolution Heino et al. (2002a, 2002b) Evolution & ICES J. Mar. Sci.

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April Northern cod case study: fisheries-induced evolution Age (years) Length (cm) Whithin 7 years, age and length at which the probability of maturating is 50% decreased by about one year and 7 cm 1987 Olsen et al. (2004) Nature

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 A widespread phenomenon SpeciesPopulation or stockData period Magnitude and rate* of evolutionary changeReference American plaice Hippoglossoides platessoides Labrador, Newfoundland1973–199922–47%12–31(S23) Grand Bank1969–200019–49%10–32(S23) St. Pierre Bank1972–199914–42%7.1–26(S23) Atlantic cod Gadus morhuaNortheast Arctic1932–199812%2.1(S11) Georges Bank1970–199826–41%15–26(S24) Gulf of Maine1970–199825–26%14–15(S24) Northern†(1977–)1981–2002– 11–27% 7–19# 11–21 (S25) (S26) Southern Grand Bank†1971–200218%9.3–9.6(S26) St. Pierre Bank†1972–200225–32%15–20(S26) Baltic1988–200321%16(S27) Atlantic herring Clupea harengusNorwegian spring- spawning 1935–20003%0.7(S28) Plaice Pleuronectes platessaNorth Sea1957– % 14% (S19) (S29) Sole Solea soleaSouthern North Sea1958–200011%4.1(S30) Jorgensen et al. (2007) Science

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April Evolutionary equilibria expected under fishing- induced selection and demographic implications Deterministic cohort-based model of phenotypic evolution

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Questions and modelling approach ∎ Is harvesting a sufficient condition to generate observed trends in life history traits? Expected life history traits’ evolutionary equilibria under fishing-induced selection ∎ What are the expected qualitative demographic implications of life history trait changes? Stock demographic characteristics at fisheries-induced evolutionary equilibria ∎ Modelling approach: deterministic cohort-based model of phenotypic evolution Life history traits: phenomenological description of growth, maturation reaction norm & size-dependent fecundity Population dynamics: deterministic age and size structured population model  Physiologically structured population model (deRoos, Metz and Diekmann 1992 ) Evolutionary dynamics: deterministic model of phenotypic evolution  Adaptive Dynamics (Metz et al. 1996; Dieckmann and Law 1996)

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Δ migration to a new environment growth trajectory Trade-off between reproduction and somatic growth rate metamorphosis Environmental variability in growth trajectories maturation reaction norm juveniles larvae adults Life history dynamics ∎ Maturation process: maturation occurs when the growth trajectory intersects with the maturation reaction norm Ernande, Dieckmann & Heino Proc Roy Soc B

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Stock Biomass Fishing Mortality positive density-dependence negative density-dependence density-independence Quotas Stock Size Harvesting and management rules ∎ Mortality rates increase because of harvesting. Three management rules: Fixed Quotas: positive density-dependence Constant Harvesting Rate: density-independence Constant Stock Size or Constant Escapement: negative density-dependence Ernande, Dieckmann & Heino Proc Roy Soc B

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Evolution under size-dependent harvesting QuotaConstant RateConstant Stock Size age (a) size (a) Unfished sizes H0H0 Ernande, Dieckmann & Heino Proc Roy Soc B

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Consequences for demography ∎ Evolutionary induced decrease in population biomass due to a decrease in adult mean size and population density. QuotaConstant RateConstant Stock Size mean adult size population biomass population density mortality Evolutionary time Proportion of original value Fishing mortality Ernande, Dieckmann & Heino Proc Roy Soc B

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April Harvest-induced evolutionary rates and potential mitigation measures Deterministic cohort-based model of quantitative genetic evolution (coupled with dynamic optimization)

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Questions and modelling approach ∎ Can we predict rates of fisheries-induced evolutionary changes? Evolutionary rates depend on selection gradient and trait’s genetic variation: underlying genetics need to be accounted for ∎ What are the potential mitigation measures at hand? There is strong socio-economic pressure to maintain fishing intensity, but gear type might be easier to manage ∎ Modelling approach: Deterministic cohort-based model of quantitative genetic evolution Life history traits: state-dependent energy allocation model describing growth, maturation and fecundity Population dynamics: deterministic model of population structured according to age, size and energy reserve  Matrix population model (Caswell 2001) Evolutionary dynamics: deterministic model of genetic evolution  Quantitative genetics model (Lande 1982)

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Food intake Stored energy Offspring Growth External factors Fishing mortality States Age Body length Stored energy Northeast Arctic cod: Energy allocation model Jorgensen, Ernande & Fiksen Evol. Appl.

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 The effect of gear selectivity: Contribution to reproduction Size (length) Reproduction …do not here Size (length) Abundance Fish reproducing here… Jorgensen, Ernande & Fiksen Evol. Appl.

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 The effect of gear selectivity: Current practice (trawls mostly) Early-maturing life history strategies have high fitness Initial distribution Jorgensen, Ernande & Fiksen Evol. Appl.

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 The effect of gear selectivity: Gillnets 186 mm mesh size Jorgensen, Ernande & Fiksen Evol. Appl.

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Evolutionary effects of gear selectivity Current Gillnet 186 mm Jørgensen (1990) Russian data (ICES) Norwegian data (ICES) No fishing during World War II – density dependence Jorgensen, Ernande & Fiksen Evol. Appl Year Mean age at maturation Length (cm) Gear selectivity

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April Fisheries-induced adaptive vs. neutral evolution and effects on genetic diversity Stochastic individual-based model of genetic evolution

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Questions and modelling approach ∎ Are there synergetic or compensatory effects between evolutionary changes in different life history traits? Multi-trait fisheries-induced evolution ∎ What is the relative importance of fisheries-induced adaptive and neutral evolution in life history trait changes? ∎ Does fishing-induced (adaptive and neutral) evolution erode genetic variability? Underlying stochastic genetics need to be accounted for ∎ Modelling approach: Stochastic individual-based model of genetic evolution Life history traits: Energy allocation model describing growth and fecundity (Quince et al.2008) + maturation reaction norm Population dynamics: emergent from stochastic events of birth and death  Individual-based model Evolutionary dynamics: emergent from an explicit multi-locus additive genetic model for life history traits + multi-locus neutral genetic model  Individual-based model

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Model structure Inheritance: Multi-loci additive/neutral genetics Life history: -Growth -Maturation -Reproduction -Mortality Bioenergetics: -Potential growth -Maturation RN intercept & slope -Adult growth investment: initial & decay Mating: -Panmixia -Random encounter -Multiple mating Density-dependent recruitment Density-dependent energy acquisition Marty, Dieckmann & Ernande. In prep

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Multi-trait fisheries-induced evolution Growth potentialAdult growth investment Growth initial investment Growth investment decay MRN interceptMRN slope Marty, Dieckmann & Ernande. In prep Smaller size-at-age Stronger fecundity-at-age Younger age at maturation Smaller size at maturation

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Erosion of genetic variance of evolving traits Growth potentialGrowth intial investment Growth investment decay MRN intercept MRN slope Marty, Dieckmann & Ernande. In prep

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 Contribution of neutral vs. adaptive evolution to genetic erosion Growth potentialGrowth intial investment Growth investment decay MRN intercept MRN slope Marty, Dieckmann & Ernande. In prep

Bruno Ernande Channel-North Sea Fisheries Unit Taking a systems approach, April 2011 ∎ Observed trends in exploited fish life history traits are compatible with expected fisheries- induced equilibria ∎ Evolutionary rates are rapid: a few decades are enough for substantial changes ∎ Maturation seem to be the most sensitive trait ∎ Fishing-induced adaptive and neutral evolution may induce irreversible erosion of genetic diversity ∎ The consequences of these evolutionary changes on stock abundance and sustainability may be strong and would be overlooked by pure population dynamics models: necessity to take evolutionary trends into account in management practices. ∎ The prevalent system of management currently, quotas, seems to be the worse management practice in terms of fisheries-induced evolution ∎ Policies on gear selectivity may be a way to mitigate fisheries-induced evolutionary changes: alleviating the selectivity on large individuals may reverse the selective pressure. Conclusions