Genetic indicators of metapopulation boundaries and dynamics in Steller sea lions: implications for recovery of an endan

Genetic indicators of metapopulation boundaries and dynamics in Steller sea lions: implications for recovery of an endangered species Greg O’Corry-Crowe Carolina Bonin Tom Gelatt Ken Pitcher Tom Loughlin John Bickham Barbara Taylor Douglas DeMaster SWFSC NMML ADF&G TAMU/Purdue

Dispersal patterns and population structure in Steller sea lions Geographic variation in population trends and ecology in Steller sea lions highlight the need for a better understanding of dispersal patterns, breeding behaviour and population structure at local, regional and macro-geographic scales Molecular genetic analysis can provide unique insights into these population parameters on both evolutionary and more contemporary time frames The focus of the current study is the use of multiple molecular genetic markers in the resolution of dispersal patterns and breeding behaviour (gene flow) at the rookery, regional and meta-population level

Dispersal patterns and population structure in Steller sea lions Earlier studies of mtDNA variation revealed evolutionary-level differentiation at macro-geographic scales Reflects isolation and subsequent expansion of Pleistocene refugial populations Eastern and Western Stock at 144°W

Sampled Rookeries EASTERN STOCK ASIAN STOCK WESTERN STOCK RUSSIA ALASKA PWS Cape Suckling BER OKH KAM CGA SEA COM WGA EAL WAL CAL BRC KUR ORE 144°W NCA JAPAN 135°W 135°E 180° Bickham et al., 1996, 1998

Dispersal patterns and population structure in Steller sea lions Earlier studies of mtDNA variation revealed evolutionary-level differentiation at macro-geographic scales Reflects isolation of two Pleistocene refugial populations Eastern and Western Stock at 144°W Phylogeographic-level differentiation was subsequently found within the Western Stock, with a break west of the Commander Islands proposed split into a Western/Central and Asian Stock These findings were recently supported by nuclear DNA analysis

Sampled Rookeries EASTERN STOCK ASIAN STOCK WESTERN STOCK RUSSIA ALASKA PWS Cape Suckling BER OKH KAM CGA SEA COM WGA EAL WAL CAL BRC KUR ORE 144°W NCA JAPAN 135°W 135°E 180° Baker et al., 2005; Harlin-Cognato et al., 2006; Hoffman et al., 2006

Part 1. Dispersal patterns and population structure within the Western Stock Differences in Steller sea lion population trends and foraging ecology exist over smaller spatial scales than the current stocks Marine ecosystem boundaries and regime shifts occur over smaller spatial and temporal scales than those generating the evolutionary-scale differences observed Hypothesis 1: is there further population structure within Alaska Steller sea lions? Hypothesis 2: is this structure related to population dynamics, ecology and marine ecosystem?

Materials and Methods Mitochondrial DNA (mtDNA) maternally inherited, non-recombination and rapidly evolving longer sequence (531bp) compared to previous studies (234bp) Microsatellite loci biparentally inherited, recombining, highly polymorphic screened 37 loci, chose 16 Sampled large numbers of pups (n=1,654) from most Alaskan rookeries (n=28) Data analysis: phylogenetic reconstruction: MSN, NJ, UPGMA population subdivision: Arlequin, Genepop (Fst, Фst), Structure 2.1 time of lineage divergence: BEAST isolation-by-distance: Arelquin (Mantel tests) assignment tests: Structure 2.1, Bayes, BAYESASS

Sampled rookeries Eastern DPS Western DPS

Results Substantial phylogeographic partitioning of mtDNA haplotypes among long established EasternDPS and Western DPS rookeries confirming an ancient divergence between these two populations Using a range of coalescent models of historical population growth as priors the time of divergence of lineages found exclusively in the Eastern or Western DPS today, was estimated at 226,000 (CV. 36,000-479,000) to 399,000 (CV. 240,00-544,000) yr. ago. Average pairwsie differences among individuals from both DPSs date population divergence at 213,000 yr.

Subdivision and dispersal within the Western DPS Fst for mitochondrial DNA Gulf of Alaska E. Aleutians Central Aleutians W. Aleutians Inter-rookery differentiation limited female dispersal

Subdivision and dispersal within the Western DPS Fst for mitochondrial DNA Gulf of Alaska E. Aleutians Central Aleutians W. Aleutians Inter-rookery differentiation limited female dispersal Regional differentiation demographic independence

UPGMA analysis based on Fst Gulf of Alaska and east Aleutian rookeries central and west Aleutian rookeries

Concern that sample size (P) and geographic separation (Fst) may have influenced this finding

Among-group ‘sliding window’ analysis to control for geographic scale and sample size

Trends in abundance (York et al., 1996, Sease & Gundmundson, 2002)

Walleye pollock salmon Atka mackeral Seal lion diet(Sinclair and Zeppelin, 2002)

Bering Slope Current Alaska Coastal Current Aleutian North Slope Current Alaskan Stream Samalga Pass = strong front in water properties along the Aleutian chain to the east : warmer, fresher, nitrate-poor, high 1o productivity to the west: cooler, more saline, nitrate-rich, low 1o productivity Ladd et al. (2005)

Conclusions: The Western DPS of Steller sea lions consists of 2 distinct metapopulations The split coincides with a strong physical and biogeographic boundary between two marine ecosystems The 2 metapopulations have separate ecologies and experienced differing trends in abundance Implications: Meets the criteria for 2 Distinct Population Segments under U.S. ESA Future research efforts should be based on this improved understanding of population subdivision and dispersal G. O’Corry-Crowe, B.L. Taylor, T. Gelatt, T. Loughlin, J. Bickham, M. Basterretche, K. Pitcher, and D.P. DeMaster (2006)

Part 2. Emigration, migration and colonization in Steller sea lions: new rookeries suggest a new paradigm The sequence of colonization of new rookeries in Southeast Alaska has been northward from: Forrester Hazy White Sisters Graves Rocks Hypothesis 3: the new rookeries were colonized by dispersing females from long-established, overcrowded Eastern Stock rookeries

Steller sea lion rookery colonization – mtDNA study Eastern Stock Western Stock Graves Rock 1998 White Sisters 1990 Hazy 1979 Forester c. 1900

Steller sea lion rookery colonization – mtDNA study Eastern lineages Western lineages Graves Rock White Sisters Hazy Forester

New sea lion rookeries have mixed origins Mimimum Spanning Tree of 130 mtDNA haplotypes Haplotypes found in the Eastern Stock Haplotypes found in the Western Stock Haplotypes found in Graves Rock and White Sisters

New sea lion rookeries have mixed origins Mimimum Spanning Tree of 130 mtDNA haplotypes Haplotypes found in the Eastern Stock Haplotypes found in the Western Stock Haplotypes found in Graves Rock and White Sisters Assignment test

Steller sea lion rookery colonization – mtDNA study 1998 1990 1979 c. 1900

Branded female from Sugarloaf on White Sisters with a newborn pup

Conclusions: Molecular genetics documented behaviour in real time Molecular genetics documented a rare event, emigration across evolutionarily distinct boundaries. Motivations for dispersal likely differed between females from the Western DPS and the Eastern DPS A unique opportunity to document the mechanisms of rookery formation Implications: Questions our understanding of the current stock boundaries Interpretation of comparative studies may need to be re-evaluated Caution when applying equilibrium models to population structure inference. Current research: Investigating the male component by screening 40 microsatellite markers

Population Structure, kinship, mating systems and dispersal patterns in Steller Sea lions Marker type: microsatellites 37 tested n=574 12 rookeries Preliminary results: 10 hypervariable loci screened for 574 sea lions 7 more to screen Individual identity substantial subdivision indicating limited interbreeding as well as limited female dispersal between the eastern DPS and western DPS Assignment tests suggest that some pups born on new rookeries in Southeast Alaska were fathered by Western males.

Future Directions Microsatellite analysis of the Aleutian Passes break Genetics of colonization and extinction on other rookeries Steller sea lion mating systems Paternity of pups on White Sisters and Graves Rocks rookeries Structure within rookeries

Acknowledgements Funding for our research has been provided by: NOAA Fisheries and the Alaska Department of Fish and Game Thanks are due to: Amy Frey, Marc Basterretche, Rich CosgroveLori Rea, Lauren Hansen, Carrie LeDuc, Steve Reilly, John Bengtson, Kaja Brix, and Bob Small And to all those souls who braved the elements and sharp teeth to collect samples Finally, to Rolf Ream for loaning me his PC after mine crashed!!!

Genetic indicators of metapopulation boundaries and dynamics in Steller sea lions: implications for recovery of an endan