Population Structure and Long-Term Decline in Three Species of Heart Urchins Abatus Spp
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Vol. 545: 227–238, 2016 MARINE ECOLOGY PROGRESS SERIES Published March 8 doi: 10.3354/meps11573 Mar Ecol Prog Ser OPENPEN ACCESSCCESS Population structure and long-term decline in three species of heart urchins Abatus spp. near-shore in the Vestfold Hills region, East Antarctica Cecilia Carrea1,*, Christopher P. Burridge1, Catherine K. King2, Karen J. Miller1,3 1School of Biological Sciences, University of Tasmania, Hobart 7001, Tasmania, Australia 2Australian Antarctic Division, Kingston 7050, Tasmania, Australia 3Australian Institute of Marine Science, Perth 6009, Western Australia, Australia ABSTRACT: Patterns of fine-scale spatial population structure in Antarctic benthic species are poorly understood. There is a high proportion of brooding species in the Antarctic benthos, and a brooding life history strategy is expected to restrict their dispersal abilities and therefore foster population structure. Additionally, genetic structuring of populations can preserve signals of his- toric processes (such as Pleistocene glaciations) on species distributions and abundances. We developed a set of 7 microsatellite markers to examine population genetic variation and infer the demographic history of 3 sympatric Antarctic sea urchin species from the order Spatangoida (Aba- tus ingens, A. shackletoni and A. philippii), all with brooding life history strategies. Samples were collected at 5 sites separated by up to 5 km, in the near-shore area surrounding Davis Station in the Vestfold Hills area of the Australian Antarctic Territory. We found evidence of a long-term population decline in all 3 species, and the estimated timing of the decline precedes anthro- pogenic activities and is compatible with long-term climate variability. Two genetic clusters in A. ingens and A. shackletoni suggest secondary contact after population differentiation in glacial refugia. Life history is not a good predictor of fine-scale population structure in these species, with gene flow possible at distances of 5 km. Finally, no evidence was found for a potential impact of pollution from Davis Station on genetic variation. The reduced effective population size observed for these Antarctic benthic species highlights their fragility and the need for conservation concern. KEY WORDS: Population structure · Demographic change · Microsatellite markers · Abatus · East Antarctica INTRODUCTION design appropriate boundaries for marine reserves that both protect diversity within and ensure disper- The recognition of the vulnerability of Antarctic sal across those boundaries (Palumbi 2003). Most of benthic biodiversity to global warming has raised the our knowledge of genetic diversity in the Antarctic urgency to improve our understanding of the biolog- benthos is from large spatial scale phylogeographic ical processes critical for effective ecosystem man- studies (ca. 1000 km) using mitochondrial DNA agement and conservation (Barnes & Peck 2008, markers (Held & Leese 2007). Intraspecific genetic Barnes & Souster 2011). In this context, the study of structure at finer scales is less well understood, par- genetic diversity and population structure is essential ticularly in Eastern Antarctica (but see Baird et al. to inform conservation initiatives, for example to 2012). Patterns of genetic population structuring can © The authors 2016. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 228 Mar Ecol Prog Ser 545: 227–238, 2016 help elucidate how species survived historical cli- species (Bradbury et al. 2008), partly because polar matic events in Antarctica, such as glaciations (All- specimens are more difficult to collect, direct meth- cock & Strugnell 2012), as well as provide insight into ods to estimate dispersal are difficult to implement at contemporary factors that may affect population high latitudes, and species-specific fast-evolving divergence. Possible factors include microevolution- genetic markers have generally been scarce for polar ary processes (e.g. selection, drift) and the species’ species (Held & Leese 2007). To our knowledge, capacity for dispersal and gene flow (Thatje 2012). there are only a few studies on fine-scale population Comparative multi-species approaches are particu- structure in Antarctic brooding invertebrates (Baird larly well suited to help elucidate the main processes et al. 2012, Hoffman et al. 2013), and both were con- shaping population genetic differentiation in the sistent with the expectation of direct development Antarctic benthos, given potential idiosyncrasies of resulting in population differentiation. Hoffman et al. individual species responses (Baird et al. 2011). (2013) found genetic population structure in the gas- The advance of grounded ice sheets across the tropod Margarella antarctica at a scale of <10 km, Antarctic shelf has been advocated as a process that and Baird et al. (2012) found limited gene flow across largely eradicated proximate benthic communities distances of 30 km in the amphipod Orchomenella during the Last Glacial Maximum (LGM) (Thatje et franklini around Casey and Davis stations in East al. 2005). Different hypotheses have been proposed Antarctica. to explain how the benthic fauna survived glacial Effective population size is a critical parameter for periods: (1) in the deep sea (Thatje et al. 2005, 2008), conservation purposes because it can help predict (2) in ice-free refugia on the Antarctic shelf (Rogers the effects of inbreeding and the loss of genetic 2007) and (3) in subantarctic islands (González- diversity due to genetic drift in natural populations Wevar et al. 2013). In a recent review of the genetic (Frankham 1995). Molecular studies using fast-evolv- patterns observed for Antarctic benthic species, All- ing markers, such as microsatellites, can help to cock & Strugnell (2012) show that populations of low detect recent changes in a population’s effective size dispersive species considered to have recolonized (Beaumont 1999). For example, studies using micro- from deep sea refugia have higher haplotype diver- satellite markers have been able to detect the genetic sity than those considered to have survived in shelf signal of population declines induced by anthro- refuges, since the latter would have experienced pogenic environmental changes 50 to 60 yr ago massive reductions in their effective sizes. Isolation (Goossens et al. 2006, Fontaine et al. 2012, Tison et in multiple glacial refugia, in combination with sub- al. 2015). In Antarctica, it has been impractical to sequent limited dispersal, has likely resulted in deep directly measure population sizes of benthic marine genetic population divergences involving cryptic invertebrates, and therefore, genetic data represent speciation in numerous taxa (Allcock & Strugnell a valuable tool in this context to test for changes in 2012). effective population size. Recently, differences in Early life history strategies (e.g. direct develop- community composition and reduced benthic biodi- ment vs. broadcaster spawning with a dispersal lar- versity were associated with environmental contami- val stage) can hinder or promote dispersal, with nation by pollutants discharged to coastal waters direct implications for population-genetic structuring adjacent to 2 stations in East Antarctica (Stark et al. (Wright 1943). Meta-analyses have supported theo- 2014). Changes in effective population size as well as retical predictions of a link between life history and in the genetic diversity of benthic species can be dispersal potential in some marine taxa (Bradbury et expected from population declines (associated with al. 2008, Selkoe & Toonen 2011), but in other compar- increased mortality) in areas impacted by pollution. ative studies, such a relationship is not clear (Riginos However, such expectations have rarely been tested, et al. 2011), indicating that the underlying mecha- but Baird et al. (2012) found reduced genetic diver- nisms are not fully understood. At small spatial sity in an amphipod associated with localized pollu- scales, the correlation between dispersal ability and tion impacts at Davis and Casey stations in East genetic structure shows a better fit than at larger dis- Antarctica. tances (Selkoe & Toonen 2011, Riginos et al. 2011). The genus Abatus (Schizasteridae, Spatangoida) For example, genetic structure was found at dis- comprises 11 known species endemic to the sub- tances as small as 300 m in a brooding sea star, while antarctic and Antarctic, 5 of which occur around the a congeneric and sympatric species with a larval coastline of Davis station (A. Miskelly pers. comm.). stage showed no significant structure (Barbosa et al. All species have direct development, and their off- 2013). Most studies have focused on lower-latitude spring are protected within the female’s brood Carrea et al.: Demographic change and population structure in Antarctic urchins 229 pouches until they are released to the environment as juveniles (Poulin & Feral 1994). Abatus cordatus (endemic to the Kerguelen Islands) shows evi- dence of population structure on spa- tial scales smaller than 1 km, as inferred by 2 allozymes (Poulin & Feral 1994) and by 3 microsatellite and 2 intron markers (Ledoux et al. 2012). Based on these studies, low dispersal capabilities for other Antarctic brood- ing Abatus species are expected. Here, we use 7 microsatellite