Population Invasion, Evolution, and Recovery: Commonalities and Potential Insights

Population Invasion, Evolution, and Recovery: Commonalities and Potential Insights Jeffrey Hutchings Department of Biology, Dalhousie University, Halifax, CANADA Centre for Ecological & Evolutionary Synthesis University of Oslo, NORWAY

Arctic char Communication of science to decisionmakers and society Demographic & evolutionary consequences of overfishing Life history evolution and phenotypic plasticity in fishes Correlates of species recovery Interactions between wild and farmed Atlantic salmon Mating systems in fishes Atlantic salmon Atlantic cod Brook trout

2015 Empirical Links Between Natural Mortality and Recovery in Marine Fishes Jeffrey A. Hutchings and Anna Kuparinen (submitted)

For small populations, recovery potential and colonization/invasion potential depend on the pattern of density dependence and on r max

For small populations, recovery potential and colonization/invasion potential depend on the pattern of density dependence and on r max r max Maximum per capita rate of population growth Negative, linear density dependence (compensation) r realised (dn/ndt) General Population Biology: Fisheries Population Biology: Allee Effect Depensation N (abundance)

r max is positively correlated with: Colonisation Probability of Introduced Species/Pop ns Individual Fitness, or Reproductive Success r max Rate and Probability of Recovery Fisheries Sustainability Reference Points

Ecology and Evolution of Fishes: Natural Selection Colonisation of new and existing habitat Different environments create opportunities for differential selection pressures

210 Million Years Ago Kristineberg Helsinki Berlin Vancouver Halifax http://jan.ucc.nau.edu/rcb7/nam.html

Helsinki Kristineberg Berlin Present day Vancouver Halifax http://jan.ucc.nau.edu/rcb7/nam.html

126,000 years ago http://jan.ucc.nau.edu/rcb7/nam.html

Land Height Increasing Land Height Decreasing

Unfished population of Atlantic cod colonised ~5,000 years ago Ne ~ 100 s of individuals (Hardie et al.,2006 CJFAS) Ogac Lake, Baffin Island Ogac Lake (July 2003/2004)

Introductions, stocking, and aquaculture can facilitate similar colonisation opportunities across considerably greater geographical scales but over much shorter periods of time. Natural environmental change has produced countless opportunities for species to colonise new habitats. When we study fish in nature, is natural selection truly the norm?

Brook trout (Salvelinus fontinalis)

Country-to-country transfers (1868-1990) Brook trout (Salvelinus fontinalis) Key condition for persistence of introduced species: evolutionary change by the colonising population in response to novel selection pressures. Data sources: Lever (1996); Jansson (2013); Froese & Pauly (2013)

1940 1950 2004 Unanticipated Insights: Introductions, Ecology, and Evolution Local Adaptation

Individuals from local/home populations have 20% higher fitness than foreign members of the same species Stocking of conspecifics: comparing home vs away populations Local populations outperform foreign populations in home environments Survival is higher in home than away environments

Introgression: Farmed and Wild Atlantic Salmon Cross Lifetime Success Wild salmon 1 BC 1 W 0.89 F 1 HyW 0.42 F 1 HyF 0.27 F 2 Hy (0.34) BC 1 F 0.31 Farmed salmon 0.02 McGinnity et al. (2003)

1940 1950 2004 Unanticipated Insights: Introductions, Ecology, and Evolution Local Adaptation: Natural Selection Against Hybridisation

Westslope cutthroat trout (Salmo clarki lewisi) Introduction/stocking of rainbow trout has resulted in hybridisation frequencies that threaten the persistence of native westslope cutthroat trout Rainbow trout (Oncorhynchus mykiss)

Brown Trout (Salmo trutta) x Atlantic Salmon (S. salar) Bream (Abramis brama) x Roach (Rutilus rutilus) Hayden et al. (2010) BMC Evol. Biol.

1940 1950 2004 Unanticipated Insights: Introductions, Ecology, and Evolution Magnitude and Rate of Evolutionary Change

Trait plasticity Rate and magnitude of evolutionary change Environment change Environment change Trait value Rate and magnitude of evolutionary change Original introduced population Subsequent naturalised populations

Phenotype Morphology Life History Behaviour Physiology Survival Gene expression 1 Phenotypic plasticity 0 Reaction norm slope and elevation can be heritable (Lande, 2009; Chevin et al., 2010). Environmental Gradient

Egg Survival 1.0 0.9 0.8 0.7 0.6 0.5 0.4 A Salmon Enhancement Programme (Fisheries & Oceans Canada) 4 8 12 Reaction Temperature norms (deg C) for survival and body size in early life Length at Emergence (mm) 39 38 37 36 35 34 33 32 4 8 12 Temperature (deg C) B Chum salmon, Oncorhynchus kisutch Beacham and Murray (1985) Can. J. Fish. Aquat. Sci. 42: 1755-1765

Hårrtjønn Øvre Mærrabottvatn Lesjaskogsvatn Aursjøen Thymallus thymallus 1880s: grayling were introduced into Lesjaskogsvatn 1910: grayling from Lesjaskogsvatn were stocked into Hårrtjønn and Øvre Mærrabottvatn (after which they dispersed into Aursjøen in the 1920s) Haugen & Vøllestad (2000) J. Evol. Biol.

Reaction norms for survival (during first 180 degree-days of exogenous feeding) Lesjaskogsvatn (9.1 o ) ( medium lake) Aursjøen (7.9 o ) ( cold lake) Time period of evolutionary change: 10-22 generations Koskinen et al. (2002) Populations experienced highest survival at temperatures most likely to be experienced in the wild Hårrtjønn (11.2 o ) ( warm lake) Haugen & Vøllestad (2000) Journal of Evolutionary Biology 13: 897-905

1940 1950 2004 Unanticipated Insights: Introductions, Ecology, and Evolution Alternative Reproductive Strategies

1959 Alternative maturation phenotypes in male Atlantic salmon Anadromous male Mature male parr

1959 Mature male parr Female

Anadromous males mature at sea 45-100cm at maturity 4-7 yr at maturity Mature male parr mature in fresh water 6-15cm at maturity 1-3 yr at maturity

Incidence of maturity (RED) for 2-year-old male Atlantic salmon parr Myers, Hutchings & Gibson (1986) Can. J. Fish. Aquat. Sci.

1959 Threshold reaction norms in male Atlantic salmon Little Codroy River, Canada Myers, Hutchings & Gibson (1986) Can J Fish Aquat Sci Anadromous male Mature male parr 1 Probability of maturing as a parr 0 Environment (growth rate, condition)

Atlantic Salmon Used for Conservation Stocking Programme Halifax 100 km

1940 1950 2004 Unanticipated Insights: Introductions, Ecology, and Evolution Human-Induced Selection Prior to Invasion/Colonisation

Male parr maturity parr maturity is heritable stocking/aquaculture selects against mature male parr

Saint John River Incidence of male parr maturity No hatchery selection: 34% 3 generations selection: 10% 5 generations selection: 7% (Debes & Hutchings. 2014. CJFAS) Stewiacke R. Origin of farmed salmon (Saint John R.) Tusket R. Salmon Farms

1940 1950 2004 What makes a successful coloniser or invader?

Some species with >90% colonisation rate Perch (Perca fluviatilis) Pike (Esox lucius) Pikeperch (Sander lucioperca) Pumpinseed (Lepomis gibbosus) Gudgeon (Gobio gobio) Common carp (Cyprinus carpio) Mozambique tilapia (Oreochromis mossambicus) Data from Froese & Pauly (2013) fishbase.org 66 species (minimum of 5 introductions attempts) ~75% of all country-tocountry introductions What makes a successful coloniser? Species with <40% colonisation rate Atlantic salmon (Salmo salar) Coho salmon (Oncorhynchus kisutch) Chinook salmon (O. tshawytscha) Cutthroat trout (O. clarki) Lake whitefish (Coregonus clupeaformis) Vendace (C. albula) Smallmouth bass (Micropterus dolomieu) Huchen (Hucho hucho)

Colonisation success success 0.2 0.4 0.6 0.8 1.0 p > 0.05 2.0 2.5 3.0 3.5 4.0 4.5 Trophic trophic level

Colonisation success success 0.2 0.4 0.6 0.8 1.0 p > 0.05 0.5 0.6 0.7 0.8 0.9 1.0 Phylogenetic diversity gendiv index (a measure of uniqueness)

Colonisation success success 0.2 0.4 0.6 0.8 1.0 p < 0.001 Colonisation probability might be related to life history and r max. r = -0.47 (p=0.0003) r max Hutchings et al. (2012) Ecological Applications 0 2 4 6 8 10 12 Age at maturity agemat (yr)

Whiting Porbeagle Atlantic cod Many depleted marine fishes show little or no recovery, despite massive reductions in fishing mortality, their primary threat. Cusk White hake Winter skate Northern wolffish Bocaccio

800 700 Northern Cod 600 Catch (1000 tonnes) 500 400 300 Catch History (1508-1991) 200 100 0 1992 1500 1550 1600 1650 1700 1750 1800 1850 1900 1950 2000 Year From: Hutchings & Myers (1995)

Northern cod today SSB=Spawning Stock Biomass A good example of Impaired Recovery But also a good example of Impaired Colonisation/Invasion potential Currently at ~18% of the population size in early 1960s 99% decline 2007 2012 2017 DFO (2016) CSAS Science Advisory Rept 2015/026

r max When Allee effects exist, a minimum number of immigrants is required before colonisation occurs. r realised weak Allee effect strong Allee effect 0 Colonisation Threshold (deterministic) Allee threshold (Stochastic) Colonisation threshold N (population size/density) K Hutchings (2015) Proc. R. Soc. B

r realised r max Further links between recovery weakpotential, Allee and effect colonisation/invasion probability. 0 strong Allee effect Colonisation Threshold (deterministic) Allee threshold (Stochastic) Colonisation threshold When Allee effects exist, a minimum number of immigrants is required before colonisation occurs. What determines whether the threshold will be exceeded? Habitat suitability Stochasticity (demographic, environmental, genetic) Number of reproductive opportunities/mates Status of native competitors, K predators and prey N (population size/density) Hutchings (2015) Proc. R. Soc. B

L infinity Length k von Bertalanffy Model Age Australia 39 recovered populations 16 non-recovered populations

(a) (b) 300 0.8 Linf (cm) 240 180 120 60 k 0.6 0.4 0.2 0 0 age at maturity (yr) (c) 16 12 8 4 0 not recovered not recovered recovered recovered length at maturity (cm) (d) 240 180 120 60 0 not recovered not recovered recovered recovered (e) maximum age (yr) 100 80 60 40 20 0 Combinations of life-history traits are far more desirable, e.g., fitness, natural mortality not recovered recovered

maximum age (yr) age at maturity (yr) Linf (cm) (a) 300 240 180 120 60 0 (c) 16 12 8 4 0 (e) 100 80 60 40 20 0 A combination of k, L inf, and L maturity 0.6 used to estimate M (natural 0.4 mortality). not recovered not recovered not recovered recovered recovered recovered k length at maturity (cm) (b) (d) 0.8 0.2 0 240 180 120 60 0 not recovered not recovered can be recovered recovered Combinations of life-history traits are far more desirable, e.g., fitness, natural mortality

Ln (Natural Mortality, M) A combination of k, L inf, and L maturity can be used to estimate M (natural mortality). Ln[k(L mat /L infinity ) -1.5 ] ~ M maturity From: Waples & Audzijonyte (2016), modified from Charnov et al. (2013)

natural mortality natural mortality at maturity (M) (M mat ) 1.5 1.5 1.2 1.2 0.9 0.9 0.6 0.6 0.3 0.3 0 0 High natural mortality (M) is generally associated with early age at maturity, short generation time, brief lifespan i.e., high r max p = 0.011 not not recovered (n=16) recovered (n=39)

Maximum per capita population growth, r max 0.2 0.4 0.6 0.8 1.0 Natural mortality (M) is positively correlated with r max p = 0.028 0.0 0.5 1.0 1.5 2.0 m1 Prediction: M is positively associated with colonisation probability. Direct estimates of natural mortality, M

Ecology and Evolution of Fishes: Natural Selection When we study fish in nature, is natural selection truly the norm? What are the 10 most studied fishes? ISI Web of Science; as of 14 March March 2017

Country-to-country transfers (1868-1990) Brook trout (Salvelinus fontinalis) Data sources: Lever (1996); Jansson (2013); Froese & Pauly (2013)

1. Rainbow Trout 2. Zebrafish 3. Atlantic Salmon (51823 papers) 4. Goldfish (13480 papers) (37447 papers) 5. Common Carp (12722 papers) (23584 papers) 6. Atlantic Cod (11424 papers) 7. Brown Trout 8. Sea Bass (8475 papers) Major introduced species 9. Medaka (6379 papers) (6491 papers) 10. Coho Salmon (6186 papers)

(5638 papers) 11. Chinook salmon 12. European eel (4799 papers) 14. Brook trout (3771 papers) 13. Guppy (3803 papers)

Invasion, Evolution, and Recovery Unanticipated Insights Local adaptation Rate of evolution Genetics of trait variability Colonisation/Invasion Probability: Predictions Correlated with age at maturity and natural mortality Depends on pattern of density dependence (e.g., Allee effects) and r max

Acknowledgements Anna Kuparinen University of Jyväskylä, Finland Robert Arlinghaus IGB-Berlin, Germany International Fish Biology Congress (Aberdeen, 2000)