ORIGINAL ARTICLE doi:10.1111/j.1558-5646.2009.00801.x DISCORDANT DISTRIBUTION OF POPULATIONS AND GENETIC VARIATION IN A SEA STAR WITH HIGH DISPERSAL POTENTIAL Carson C. Keever,1,2 Jennifer Sunday,1 Jonathan B. Puritz,3 Jason A. Addison,2,4 Robert J. Toonen,3 Richard K. Grosberg,2 and Michael W. Hart1,5 1Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada 2Center for Population Biology, College of Biological Sciences, University of California, Davis, California 95616 3Hawaii Institute of Marine Biology, University of Hawaii, P.O. Box 1346, Kaneohe, Hawaii 96744 5E-mail: mwhart@sfu.ca Received November 10, 2008 Accepted July 19, 2009 Patiria miniata, a broadcast-spawning sea star species with high dispersal potential, has a geographic range in the intertidal zone of the northeast Pacific Ocean from Alaska to California that is characterized by a large range gap in Washington and Oregon. We analyzed spatial genetic variation across the P. miniata range using multilocus sequence data (mtDNA, nuclear introns) and multilocus genotype data (microsatellites). We found a strong phylogeographic break at Queen Charlotte Sound in British Columbia that was not in the location predicted by the geographical distribution of the populations. However, this population genetic discontinuity does correspond to previously described phylogeographic breaks in other species. Northern populations from Alaska and Haida Gwaii were strongly differentiated from all southern populations from Vancouver Island and California. Populations from Vancouver Island and California were undifferentiated with evidence of high gene flow or very recent separation across the range disjunction between them. The surprising and discordant spatial distribution of populations and alleles suggests that historical vicariance (possibly caused by glaciations) and contemporary dispersal barriers (possibly caused by oceanographic conditions) both shape population genetic structure in this species. KEY WORDS: Asterinidae, ATPS, effective population size, GPI, life history, planktotrophy. Explaining the origin and persistence of large geographical dis- continuities in species distributions, such as the antitropical dis- tributions of many temperate-zone animals and plants, is one of the original goals of evolutionary ecology (Darwin 1859 Ekman 1953 Briggs 1987 Wiley 1988 Lindberg 1991). Such range disjunctions may be initiated and maintained by a com- plex combination of factors, encompassing extrinsic geological and climatic barriers to dispersal and colonization, and intrinsic biological properties of organisms including habitat preferences 4 Current address: Department of Biology, University of New Brunswick, Fredericton, NB E3B 5A3, Canada and dispersal capabilities (Schwaninger 2008). Dispersal barriers such as mountain ranges or climatic effects associated with Pleis- tocene glacial cycles (DeChaine and Martin 2006 Knowles and Carstens 2007) are well-known determinants of the geographical distribution both of populations and of genetic variation in ani- mals and plants of the Northern Hemisphere (Hewitt 1996 Riddle 1996 Byun et al. 1997 Knowles 2001 Lovette 2005). The intrinsic potential of some organisms to traverse physi- cal and geological features that are barriers to dispersal for other species (e.g., Lessios et al. 1998) is arguably greatest among sessile and sedentary marine animals that have prolonged de- velopment of feeding planktonic (planktotrophic) larvae. Direct 3214 C 2009 The Author(s). Journal compilation C 2009 The Society for the Study of Evolution. Evolution 63-12: 3214���3227

PATIRIA MINIATA POPULATION STRUCTURE estimates of realized dispersal in species with planktotrophic development are restricted for logistical reasons to cases in which realized dispersal is limited to small spatial scales (e.g., Knowlton and Keller 1986), but inferences based on oceanogra- phy and larval duration suggest that realized dispersal can exceed 103���104 km per generation (Scheltema 1986 Shanks et al. 2003). Numerous lines of evidence suggest a correlation between the evolutionary gain or loss of planktonic larval development and the magnitude or geographical scale of neutral genetic differenti- ation among marine animal populations (Arndt and Smith 1998 Bohonak 1999 Kyle and Boulding 2000 Grosberg and Cun- ningham 2001 Hellberg et al. 2002 Kelly and Eernisse 2007 Teske et al. 2007). However, this trend conflicts with a con- spicuous minority of other studies that reveal strong phylogeo- graphic breaks in spite of prolonged planktonic larval develop- ment, or large differences in population genetic structure between sympatric species with similar larval dispersal potential (Benzie 1999 Swearer et al. 1999 Forward et al. 2003 Marko 2004 Hickerson and Cunningham 2005 Crandall et al. 2008 Hamilton et al. 2008). The concordance between the geographical distributions of populations (including patterns such as range disjunctions) and of population genetic variation (phylogeographic breaks) can be used to test biogeographic hypotheses (Avise 2000). Range dis- junctions that coincide with phylogeographic breaks are consis- tent with the effects of geological or physical processes (like glaciations) that limit dispersal, and implicate dispersal barriers in the origin of the disjunct range (e.g., Munoz-Salazar �� et al. 2005). Alternatively, range disjunctions that do not correspond to phylogeographic breaks suggest gene flow across the disjunction, and implicate ecological effects such as the distribution of suit- able habitat, habitat selection by recruiting propagules, juvenile mortality, or recent extirpation (rather than dispersal barriers) in the origin of the disjunct range. Comparative analyses of sym- patric species that share the same range disjunction have revealed mixtures of results that match both of these patterns (Bernardi et al. 2003 Ayre et al. 2009). Here we use a large suite of mitochondrial and nuclear ge- netic markers to test the strength of the concordance between biogeographic and phylogeographic discontinuities in the bat star Patiria miniata (formerly Asterina miniata O���Loughlin and Waters [2004]) from the northeast Pacific. Bat stars are abundant omnivores in intertidal and shallow subtidal marine communities in sheltered waters of southeast Alaska, British Columbia, central and southern California, and Baja California (Fisher 1911 Lam- bert 2000), but are strikingly rare in or absent from the outer coasts of Washington, Oregon, and northern California between Cape Flattery, WA (48���38 N, 124���71 W) and Cape Mendocino, CA (40���26 N, 124���24 W) (Kozloff 1983) (Fig. 1). The north- ern part of the P. miniata range includes the transition between Figure 1. Haplotype network for Patiria miniata mtDNA se- quences. Each symbol represents a unique sequence (28 total). The area of each circle (and of the segments in each pie diagram) is proportional to haplotype frequency (n = 1���120). Lines between symbols indicate single substitution differences between haplo- types (the small open symbol indicates one missing haplotype inferred for two sequences that differed by two substitutions), and are not proportional to genetic distance between haplotypes. Color coding indicates the origin of each private haplotype (solid circles) or the frequency of shared haplotypes (pie diagrams) in each region indicated in the map at right: Alaska (AK, dark blue) and Haida Gwaii (HG, cyan) to the north of Queen Charlotte Sound (QCS) Vancouver Island (VI, green) and California (CA, red) to the south. Black rings on the map show approximate locations of sam- ple sites (some indicate 1 locations separated by small distances see Table 1). The arrows show the approximate location of the di- vergence of the North Pacific Current. The hatched shading shows the P. miniata range disjunction. the Oregonian and Aleutian zoogeographical provinces (Briggs 1974), and the range disjunction includes the southern extent of the Wisconsin glaciation on the Pacific coast of North America at about 48���N latitude (Pielou 1991). Comparative population genetic studies of this community (Hellberg 1996 Arndt and Smith 1998 Burton 1998 Rocha- Olivares and Vetter 1999 Kyle and Boulding 2000 Dawson EVOLUTION DECEMBER 2009 3215