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The Tales of Two Geckos: Does Dispersal Prevent Extinction In Molecular Ecology (2007) 16, 3299–3312 doi: 10.1111/j.1365-294X.2007.03352.x TheBlackwell Publishing Ltd tales of two geckos: does dispersal prevent extinction in recently fragmented populations? M. HOEHN,*† S. D. SARRE† and K. HENLE* *Helmholtz Centre for Environmental Research — UFZ, Department of Conservation Biology, Permoserstrasse 15, 04318 Leipzig, Germany, †Applied Ecology Research Group, University of Canberra, ACT 2601, Australia Abstract Although habitat loss and fragmentation threaten species throughout the world and are a major threat to biodiversity, it is apparent that some species are at greater risk of extinction in fragmented landscapes than others. Identification of these species and the characteristics that make them sensitive to habitat fragmentation has important implications for conser- vation management. Here, we present a comparative study of the population genetic structure of two arboreal gecko species (Oedura reticulata and Gehyra variegata) in fragmented and continuous woodlands. The species differ in their level of persistence in remnant vegetation patches (the former exhibiting a higher extinction rate than the latter). Previous demographic and modelling studies of these two species have suggested that their difference in persistence levels may be due, in part, to differences in dispersal abilities with G. variegata expected to have higher dispersal rates than O. reticulata. We tested this hypothesis and genotyped a total of 345 O. reticulata from 12 sites and 353 G. variegata from 13 sites at nine micro- satellite loci. We showed that O. reticulata exhibits elevated levels of structure (FST = 0.102 vs. 0.044), lower levels of genetic diversity (HE = 0.79 vs. 0.88), and fewer misassignments (20% vs. 30%) than similarly fragmented populations of G. variegata, while all these parameters were fairly similar for the two species in the continuous forest populations (FST = 0.003 vs. 0.004, HE = 0.89 vs. 0.89, misassignments: 58% vs. 53%, respectively). For both species, genetic structure was higher and genetic diversity was lower among fragmented populations than among those in the nature reserves. In addition, assignment tests and spatial autocorrelation revealed that small distances of about 500 m through fragmented landscapes are a barrier to O. reticulata but not for G. variegata. These data support our hypothesis that G. variegata disperse more readily and more frequently than O. reticulata and that dispersal and habitat specialization are critical factors in the persistence of species in habitat remnants. Keywords: continuous, dispersal, effective population size, geckos, generalist, habitat fragmentation, microsatellites, population genetics, specialization Received 9 December 2006; revision accepted 20 March 2007 landscapes than others. Identification of these species and Introduction the characteristics that make them sensitive to habitat Habitat loss and fragmentation threaten species through- fragmentation has important implications for the manage- out the world and are a major threat to biodiversity ment of species as well as contributing to our understanding (Groombridge 1992; WCMC 1992). When formerly of ecological and evolutionary theory (Sarre et al. 1995; contiguous vegetation becomes fragmented through land MacNally et al. 2000; Davies et al. 2000, 2001, 2004; Henle clearing, small isolated populations will result for many et al. 2004a, b; Schmuki et al. 2006). species. Emerging empirical evidence suggests that some Dispersal between an individual’s birthplace and that of species are at greater risk of extinction in fragmented its offspring is one of the most important life-history traits in species persistence (Koenig et al. 1996; Clobert et al. 2001; Correspondence: Marion Hoehn, Fax: +49 341 235 3191; E-mail: Sumner et al. 2001). Dispersal will usually result in gene [email protected] flow, the movement and integration of alleles from one © 2007 The Authors Journal compilation © 2007 Blackwell Publishing Ltd 3300 M. HOEHN, S.D. SARRE and K . HENLE population into another. Gene flow protects small popula- stochasticity also show contrasting expectations for the tions from processes such as reduction in the number of two species (Sarre et al. 1996; Wiegand et al. 2001, 2002). alleles, reduction in heterozygosity, and reduction in Whereas rates of persistence observed were lower for O. genetic diversity through genetic drift and inbreeding reticulata than those predicted by the population viability (Frankham et al. 2002; Keller & Waller 2002). Although model, the opposite was the case for G. variegata. One of dispersal used to be difficult to study, genetic markers the reasons for the discrepancies between predicted and provide a powerful tool for obtaining indirect estimates of observed distributions may be that the models did not dispersal and gene flow in natural populations. Recent include an expectation of dispersal between remnants for advances in statistical techniques and the analysis of micro- either species. While the dispersal capability of O. reticulata satellite data promise to simplify studies of dispersal and is believed to be low, pitfall trapping and anecdotal evidence colonization. For instance, assignment testing can improve suggest that movement by G. variegata is also infrequent the resolution of dispersal patterns by assigning individu- (Sarre et al. 1995; R. How, personal communication). als to their most likely population of origin (Paetkau et al. Nevertheless, occasional longer-distance dispersal is 1995; Rannala & Mountain 1997; Cornuet et al. 1999; Pritchard known for G. variegata (Moritz 1987; K. Henle & B. Gruber, et al. 2000). Like F-statistics, the basis of assignment protocols unpublished data.). Sarre et al. (1996) suggested that the is an estimate of the allele frequency within populations discrepancy between the observed and modelled persistence and therefore requires an a priori identification of popula- rates could be best explained by greater rates of movement tion boundaries. In contrast, analytical methods that do not for G. variegata than for O. reticulata. require information about population boundaries, such as To investigate further this dichotomy of responses to isolation-by-distance analysis and spatial autocorrelation, fragmentation, we used microsatellite DNA markers to can use genetic and geographical information to describe compare the genetic structure and rates of dispersal in the dispersal and genetic spatial structure in a two-dimensional two gecko species. Our expectation is that the high level of landscape (Rousset 1997; Peakall & Smouse 2001; Double persistence exhibited by G. variegata is a result of a higher et al. 2005). dispersal rate compared with O. reticulata. Thus, we pre- Here, we present a comparative study of the genetic dicted higher levels of genetic differentiation and lower rates structure of two gecko species in fragmented and continuous of dispersal among O. reticulata than among G. variegata woodlands. The species occur sympatrically, but have populations. We surveyed the genetic structure in fragmented responded differently to the fragmentation of their wood- and continuous populations of these two species to test our land habitat. Gehyra variegata (tree dtella) is abundant and hypotheses. In addition, we expected a loss of genetic widespread throughout the southern half of Australia. It is diversity and a higher level of genetic structure for both a habitat generalist, and can be found on trees, logs, fallen species in habitat fragments. timber, shrubs, rocks, and in highly disturbed habitat. Oedura reticulata (reticulated velvet gecko) is endemic to Materials and methods the southwest of Western Australia and is a habitat specialist. It is limited in its habitat range, being exclusively arboreal Study area and sampling and restricted to smooth-barked Eucalyptus woodlands. Both species have been subjected to severe population The study area was located between Kellerberrin and fragmentation in the Western Australian wheatbelt, where Trayning in the Western Australian wheatbelt (Fig. 1). numerous very small populations persist in patches of Large areas of native vegetation have been removed from woodland surrounded by land used for wheat crops. In the region and replaced by agricultural crops, pastures, summer, the intervening matrix is often reduced to sparse and livestock. Since 1900, approximately 93% of the original stubble or even predominantly bare earth (How & Kitchener vegetation has been cleared and the remnant vegetation is 1983; Kitchener et al. 1988; Sarre 1995a, b, 1998; Sarre et al. distributed over thousands of patches of varying size 1995). (Saunders & Hobbs 1991; Hobbs 1993; Saunders et al. 1993). In a previous empirical study, Sarre et al. (1995) demon- Tissue samples were collected from the two gecko spe- strated that G. variegata showed a markedly higher persistence cies during the summer months, from November 2000 than O. reticulata in habitat remnants (97% remnant occu- until March 2001, in December 2003, and in November pancy vs. 72%). In addition, studies 10 years apart (1991 2005. A total of 345 Oedura reticulata individuals from six and 2001) documented extinction of O. reticulata in three of habitat fragments and six locations in two nature reserves 33 habitat remnants, whereas G. variegata has persisted at and a total of 353 Gehyra variegata individuals from seven comparable population sizes in all 33 remnants over the habitat fragments and six locations in two nature reserves
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