RESEARCH REPORT doi: 10.1111/j.1442-8903.2009.00490.x Monitoring movement into and through a newly planted rainforest corridor using genetic analysis of natal origin
By David Paetkau, Ella Va´zquez-Domı´nguez, Nigel I. J. Tucker and Craig Moritz
This work was undertaken at a time when David Summary Genetic analysis of individual origins works best with populations that are Paetkau and Ella Vázquez-Domínguez were Post- genetically distinct but which exchange a high rate of immigrants, conditions that don’t nor- doctoral fellows with Craig Moritz at the Depart- mally coexist since immigration acts to prevent the accumulation of genetic differences. We ment of Zoology and Entomology, University of provide empirical results from a newly constructed habitat linkage to illustrate the unique Queensland, St. Lucia 4072, Qld, Australia. David is suitability of such analysis to monitoring the re-establishment of connections between previ- now President and Molecular Artificer with Wild- ously isolated populations. Donaghy’s Corridor links a previously isolated 498 ha fragment of life Genetics International (Box 274, Nelson, BC, rainforest to an adjacent 80 000 ha of intact forest. Starting in the final year of the planting Canada V1L 5P9; Tel +1-250-352-3563; Email: programme that established the corridor, we trapped two species of native small mammals, [email protected]). Ella is a Research Pro- the Bush Rat (Rattus fuscipes) and the Cape York Rat (Rattus leucopus), within and nearby fessor with the Instituto de Ecologı´a, Universidad the linkage. We used genetic data from ear clippings to determine which side of the corridor Nacional Auto´noma de Me´xico (Ap. Postal 70-275, individual animals originated from, and by comparing this information to trap locations, we Ciudad Universitaria, Me´xico DF 04510, Mexico); identified 16 long-distance movements through the corridor. As genetic analysis of origins and Craig is a Professor at the Museum of Verte- allowed movements to be detected from a single capture event and as it reflected movement brate Zoology, University of California (Berkeley, CA since birth, this approach yielded considerably more data than capture records alone. The 94720-3160, USA). Nigel, at the time coordinating combination of movement and capture records allowed species-specific assessment of corri- the Donahy’s Corridor restoration project, is now dor function, revealing that the use and occupation of the corridor was higher for Bush Rat Director and Principle with Biotropica Australia (PO than for Cape York Rat and was neither symmetrical nor uniform. Long-distance movements Box 866, Malanda, Qld, Australia). The study was through the corridor were most common immediately after habitat restoration, dropping off as undertaken with the goal of developing individual- the reconstructed habitat was colonized. based genetic techniques that would yield practical information on current landscape usage; with Dona- Key words: dispersal, genetic assignment, microsatellite, wildlife corridor. ghy’s Corridor providing a testing ground for these genetic methods.
event, may have potential to bridge this balance between genetic drift and migra- Introduction gap in some population systems. tion is near equilibrium, genetic analysis of ispersal is a focal parameter in popula- Genetic assessment of origins has a pro- origins is frustrated by the paradox that Dtion genetics (Wright 1951) and land- ven capacity to assign individuals to their migration limits the very population differ- scape ecology (Wiens 1997) and this population of origin when those popula- entiation which enables the identification intersection has encouraged a search for tions experience little or no ‘migration’ of immigrants (e.g. Manel et al. 2002; Pae- practical management applications of (the geneticist’s term for any movement of tkau et al. 2004); if allele frequencies in genetic movement data. Traditional popu- genes between populations). This capacity two populations have been homogenized lation genetics, which treats populations has been applied to such problems as iden- through gene flow, then the members of as the units of analysis and uses models tifying movement between and coloniza- those populations cannot be distinguished that assume long-term equilibrium, does tion of habitat patches (Eldridge et al. using genetics. not generate the fine-scale, individual- 2001; Berry et al. 2005), identifying the ori- One context in which movement data based, contemporary movement data that gin of hunted animals in the context of have been particularly sought after but dif- are provided by established field tech- management and law enforcement (Manel ficult to obtain (Rosenberg et al. 1997; niques, and that are generally required for et al. 2002; Maudet et al. 2002), or assign- Beier & Noss 1998) is in evaluating the effi- practical assessment of landscape function. ing harvested fish in mixed fisheries to cacy of restored habitat linkages (wildlife Genetic analysis of individual origins (Pae- their breeding stocks (Primmer et al. 1999; corridors) for re-establishing connectivity. tkau et al. 1995; Rannala & Mountain Roques et al. 1999). The approach has Such linkages have been identified as one 1997; Cornuet et al. 1999; Pritchard et al. even documented movement between of the major tools of conservation biology 2000; Guinand et al. 2002), which seeks to conterminous but discretely defined popu- (Tewksbury et al. 2002), but the lack of identify individuals’ place of birth and thus lation fragments in Grizzly Bears (Ursus data surrounding their effectiveness has to detect lifelong movements by individu- arctos;Proctoret al. 2005). However, in been a source of criticism (e.g. Simberloff als that are known from a single capture most population systems, where the et al. 1992).
210 ECOLOGICAL MANAGEMENT & RESTORATION VOL 10 NO 3 DECEMBER 2009 ª 2009 Ecological Society of Australia RESEARCH REPORT
From a genetic perspective, the popula- Our goal was to test empirically rainforest-specialist species would not tions on either side of a new habitat link- whether the unique combination of popu- have crossed between Gadgarra and Lake age have been drifting apart in isolation, lation parameters associated with new hab- Barrine since 1931, when the intervening and the role of the linkage is to re-establish itat linkages would provide a practical forest was removed (Tucker 2000a). gene flow. The genetic drift that precedes application of direct genetic analysis of The monitoring program that was habitat restoration creates a scenario with movement. The linkage that we selected applied at Donaghy’s Corridor involved greater initial population differentiation for this purpose (Donaghy’s Corridor) is birds, reptiles, amphibians, invertebrates than would eventually be expected if located in the Wet Tropics World Heritage and mammals (Tucker 2000b). We elected the restoration successfully re-establishes Area of northern Queensland, Australia, to study two species of small, native mam- movement. This unusual and transient and was established between 1995 and mals, Cape York Rat (Rattus leucopus)and combination of relatively high population 1998 along a 1.2-km riparian strip (Tucker Bush Rat (R. fuscipes). These animals were differentiation and – one hopes – relatively 2000a; Fig. 1). The purpose of Donaghy’s selected because they had been captured high-frequency movement could endow Corridor was to reconnect the 498 ha Lake in large enough numbers to enable a genetic assignment methods with the Barrine section of Crater Lakes National genetic study to be undertaken without capacity to detect individual movements. Park with the 80 000 ha of contiguous initiating a new trapping program, and For example, such an approach was used tropical rainforest in the Gadgarra Forest because we expected these forest species to show more or less unidirectional move- section of Wooroonooran National Park. to have been affected by the fragmentation ment into and through a habitat corridor The previously continuous forest in this event. Neither species is noteworthy for its from a rapidly expanding Black Bear region was fragmented during clearing for conservation priority. (U. americanus)population(Dixonet al. agricultural settlement in the early 1900s, The study species are difficult to distin- 2006). and it was our expectation that many guish in the field, but one or both can be found in the wet eucalyptus forest that occurs adjacent to the rainforest, although they are more abundant in the latter (Wil- liams et al. 2002). It has been suggested that the Cape York Rat is more tolerant of forest edge than its congener, and that small forest fragments tend to contain only one or the other of these two species (Lau- rance 1994). Our laboratory analysis made use of highly variable microsatellite markers, and the statistical interpretation of the resulting data employed several of the rapidly evolv- ing methods that use genetic data to draw inference about individual origins.
Methods Donaghy’s Corridor Donaghy’s Corridor was established by planting approximately 18 000 rainforest plants (103 species) in four blocks, one block planted each year between 1995 and 1998 (Tucker 2000a,b; Tucker & Simmons 2009; Fig. 1). The linkage varies between 70 m and 120 m in width, and is bounded on either side by a 15-m windbreak ⁄ agro- forestry zone of Hoop Pine (Araucaria Figure 1. Donaghy’s Corridor. This habitat linkage was planted in four sections between 1995 ). The 1995 planting and 1998. It follows a natural stream course and includes areas of natural regrowth in which habitat cunninghamiana restoration was encouraged by excluding cattle, but where no planting was undertaken. Trapping joined Gadgarra to a small fragment of for- grids in the open pasture on either side of the corridor served as controls. Samples from the area est that had regenerated since the initial planted in 1996–1998 were grouped for genetic analysis (DCLB), as were samples from the 1995 clearing event, but in which the under- and Remnant trapping grids (DCGF). story had been largely destroyed by cattle.
ª 2009 Ecological Society of Australia ECOLOGICAL MANAGEMENT & RESTORATION VOL 10 NO 3 DECEMBER 2009 211 RESEARCH REPORT
During the next 3 years, three blocks were We used GeneClass 2 (Piry et al. 2004) Statistical analysis planted to connect Lake Barrine with Gad- for statistical testing of the immigrant sta- garra via the 1995 planting and remnant The data were first analyzed with Structure tus of specific individuals. This program sections. For the purposes of the current 2.1 (Pritchard et al. 2000), in which requires reference data from pre-defined analysis, the 1995 planting and the rem- genetic clusters are identified without ref- groups of individuals, and we explored nant were grouped into an area labelled erence to non-genetic information (i.e. cap- two different ways of identifying these
DCGF, and the three plantings proximal to ture location). This program requires that groups: using capture location (Lake Bar-
Lake Barrine were grouped as DCLB. the user input the number of populations rine + DCLB versus Gadgarra + DCGF)or Quarterly trapping sessions were initi- into which the data should be clustered using the clusters identified by Structure at ated in April 1997 (Tucker 2000b). Two (K). In many studies, Structure is used to K =2(q < 0.3 versus q > 0.7). The cutoff trapping grids were established in each of identify the most likely value of K, but our for the Structure-defined groups was sub- Lake Barrine and Gadgarra Forest, one at study was based on a linear landscape fea- jectively based on the observation that a the edge of the established forest and ture with 2 ends (thus K = 2) and our less stringent cutoff would include individ- one approximately 400 m from the edge interest in Structure was to apportion each uals that were clearly outliers relative to (Fig. 1). Trapping grids were established in individual’s genetic ancestry between the the identified modes (Fig. 2) whereas stric- each section of the linkage, such that DCLB two ends of the corridor. All analyses used ter values would compromise the Bush Rat contained three grids (96 ⁄ 97 ⁄ 98) while the admixture model, which assumes that sample size for Gadgarra Forest. We found
DCGF contained two (remnant and 1995 hybrid individuals may occur. For each spe- that an implausibly high number of immi- planting). Trapping grids were also estab- cies, we selected the allele frequency grants were identified when using any- lished in the open paddocks on either side model (Falush et al. 2003) that resulted in thing but the most conservative methods of the linkage to test for the presence of the largest proportion of individuals with (those recommended by Paetkau et al. the study species in non-forested habitat. values of q (estimated proportion of ances- 2004) for resampling and probability calcu- Each trapping grid consisted of 20 ‘Elliot’ try in population 1) in the upper and lower lations. These methods involve the sam- box traps set at 5-m intervals around the deciles. The burn-in and run periods were pling of gametes instead of alleles, to perimeter of a square (Tucker & Simmons 50 000 and 500 000 steps, respectively, preserve linkage disequilibrium, and ana- 2009). Recaptures were confirmed by ear for Cape York Rat, and 200 000 and lyzing simulated data in groups of the same tags or, when tags had been lost, by match- 2 000 000 steps, respectively, for Bush size as the study data set. We tested the sta- ing genotypes (all animals that were Rat. The analysis was repeated 10 times tus of each individual as immigrant or resi- known to be unique based on field data per species, and q for each individual taken dent in its capture location using a test had unique genotypes). as the mean across 10 runs. statistic that was the ratio of genotype like- The collection of ear clippings for Structure contains an option to assign lihoods in the two reference populations. genetic analysis was initiated during the statistical significance to the immigrant sta- Basic tests of how genetic variation was April 1998 trapping session, and contin- tus of specific individuals if the user sup- partitioned within and between popula- ued through the January and April ses- plies capture location. We did not use this tions were made using Genepop 3.4 on sions of 2000. The study species could option because we found it to be sensitive the web (
Laboratory methods The microsatellite markers and analysis Bush Rat conditions were as described by Hinten et al. (1999) and Va´zquez-Domı´nguez 10.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1 et al. (2001). Of these 10 markers, RfgJ5 Estimated Proportion of Ancestry in Lake Barrine (q) was monomorphic in Cape York Rat and Figure 2. Estimate of ancestry (q;Pritchardet al. 2000), averaged across 10 runs, for individual was not used in any statistical analysis animals from two study species. Symbols indicate capture location: Lake Barrine open diamonds; involving this species. Only samples that DCLB closed diamonds; DCGF closed triangles; Gadgarra Forest open triangles. Long-distance produced unambiguous genotypes for all immigrants are indicated by diamonds with q < 0.3, or triangles with q > 0.7. Identification numbers markers were used in the analysis. are given for four animals that are discussed in text.
212 ECOLOGICAL MANAGEMENT & RESTORATION VOL 10 NO 3 DECEMBER 2009 ª 2009 Ecological Society of Australia RESEARCH REPORT between-population genetic differentiation Cape York Bush Rat populations per species (i.e. that K =3)is (F ) if it pools animals from two source Rat not supported by our data. ST 20 15 populations (Wahlund 1928). We found In the Cape York Rat, the ‘detection of 10 clear evidence that individuals captured in 10 F0 immigrants’ analysis in GeneClass (refer- a given location came from two genetically 5 ence populations based on capture loca- distinct source populations (below), so we 0 0 tion) identified one individual that was performed the Genepop analysis using the 20 15 captured in Gadgarra (O140; Fig. 2) but groups identified by Structure (q < 0.3 ver- 10 that had origins in Lake Barrine (P < sus > 0.7) rather than groups identified 10 0.001), and one individual (64) with ori- q 5 by capture location. gins in Gadgarra that apparently moved 0 0 through DC to its capture location in 20 15 GF DCLB (P < 0.001). Two individuals with Results 10 10 intermediate values of q (504 & 613) were Trapping 2000 1999 1998 5 rejected at a lower value of significance 0 (P = 0.023 & 0.011), which can only be Sample sizes (individuals with complete 0 Capture Location taken as a suggestive result given the num- genotypes only) for each species are L to R: GF DCGF DCLB LB ber of individuals tested. We wondered if shown in Table 1, and broken down by Figure 3. Number of captures broken down these two animals might be F1 hybrids time and location in Figure 3. While by species, location, year and genetic assign- with one parent from either end of the cor- genetic samples were not taken during the ment. Gray indicates genetic origin in Gadgarra ridor, and tested this hypothesis by moving 1997 trapping sessions, there were no cap- Forest (GF) and black origin in Lake Barrine these individuals into the Gadgarra refer- tures of either species in DC that year. (LB). Individuals with intermediate values of q LB ence population and repeating the Trapping stations in the open paddocks on (Fig. 3) were assumed to originate in their cap- analysis. They were rejected from this pop- either side of the linkage produced no cap- ture location, except for two putative F1 hybrids ulation with a higher level of significance tures of either study species. that are identified by hatched shading. Recap- tures at the same site in the same year are (P = 0.003 & 0.010 respectively). Another Data analysis excluded. There were no captures of either spe- four individuals had probabilities of non- cies in DC in 1997. immigrant status in the range of 0.01 to Structure produced the tightest clustering LB 0.05, although these animals did not stand with the independent allele frequencies out in the Structure analysis. Assuming that model in the Cape York Rat, whereas Bush higher for Bush Rat, with one individual the critical values were accurate, we Rat genotypes clustered more strongly showing a range of 0.22 between extreme would have expected 3 or 4 individuals in with correlated allele frequencies. The per- values of q across 10 runs, 67 of 72 individ- our sample of 69 to have probabilities in centage of animals with q <0.1orq >0.9 uals had run to run variation below 0.1. this range, even if none were immigrants was 90% for Cape York Rat and 71% for Run-to-run variation was highest for the (Type I error). Bush Rat (Fig. 2). Only 6 individuals across few individuals with intermediate q (i.e. The Bush Rat Structure results appeared 2 species had 0.3 < q < 0.7, perhaps sug- those with possible hybrid ancestry), none to identify 14 long-distance immigrants, gesting hybrid ancestry. There was no of which was a putative immigrant. Each including five animals of Gadgarra origin meaningful variation in q across 10 runs of of the 10 runs of Structure identified the that were captured in Lake Barrine, 6 that Structure for Cape York Rat, with no two same putative immigrants in both species. crossed the linkage in the opposite direc- results for any given individual differing by Our interest was in apportioning tion, and three that were captured in the >0.02. While run-to-run variation was genetic ancestry between two populations section of corridor that was furthest from (Gadgarra and Lake Barrine), and the pri- their apparent population of origin mary partitions in the genetic data (i.e. (Fig. 2). Of these 14 animals, five were results at K = 2) straddled the landscape identified by GeneClass as immigrants Ta ble 1 . Sample sizes (number of individu- feature of interest. We did, however, per- (P<0.01), and only two had probabilities als with complete multilocus genotypes) and form exploratory runs of Structure at in excess of 0.05. mean HE across nine or ten microsatellite markers per species. Capture locations are K = 3. In each species, these runs had While the GeneClass results confirmed Gadgarra Forest (GF), Donaghy’s Corridor effectively no impact on one of the two the status of some putative Bush Rat immi- (DC) and Lake Barrine (LB) groups that were identified at K =2,but grants, we were concerned that the large split the ancestry of individuals assigned to number of immigrants would compromise Species Sample H E the other end of the corridor (Lake Barrine the power of this analysis by mixing the sizes for Cape York Rat, Gadgarra for Bush Rat). reference populations. Reasoning that the GF DC LB GF LB These newly split populations contained Structure results represented a better parti- Bush Rat 32 20 22 0.64 0.73 implausibly high proportions of hybrids, so tion of the local genetic variation than did Cape York Rat 23 12 36 0.73 0.82 the hypothesis that we sampled 3 distinct capture locations (compare FST values,
ª 2009 Ecological Society of Australia ECOLOGICAL MANAGEMENT & RESTORATION VOL 10 NO 3 DECEMBER 2009 213 RESEARCH REPORT below), we set up a file using reference long-distance movement (Cape York Rat Discussion populations defined by Structure, and then 64; Fig. 2), it was only through genetic tested each of the 14 putative immigrants The level of genetic differentiation that we analysis that we could assign polarity to one at a time by moving them to their cap- observed between Lake Barrine and Gad- this movement event, identifying the indi- ture population and repeating the analysis. garra Forest (FST 0.1) is indicative of low vidual as returning to its natal population Five individuals with intermediate values levels of population interchange ( 2 following a long-distance foray rather than of q (Fig. 2) were excluded from this migrants per generation; Wright 1951), being an immigrant. analysis. These five were conservatively even under the conservative assumption As this comparison shows, the genetic assumed to be outlier non-immigrants. The that this differentiation is not increasing, as results were a far richer source of move- highest probability that was returned was it would be if the populations became sep- ment data than the field data alone. These 0.004, with the remaining 13 results giving arated in 1931 when the intervening forest results are particularly encouraging given P < 0.001. Clearly all 14 of these individu- was removed. Combined with the absence the modest number of markers that we als had genetic origins on the side of DC of captures in the open pasture sites, or in analyzed, since many of the species to that was furthest from their respective DCLB in 1997, this provides clear evidence which we would anticipate our methods capture locations. that these populations experienced little being applied would be of high conserva- The test of population differentiation connection prior to construction of the tion priority, and could attract resources (Genepop) returned P-values of zero for habitat linkage. Following the establish- for the analysis of more markers. at least one marker in each species, creat- ment of a habitat linkage between these The preceding discussion satisfies our ing a combined (across loci) chi-square forested areas, we identified long-distance main objective of illustrating the suitability value of infinity. This simply confirms that movements by 16 individuals in two spe- of genetic analysis of origins in situations the two clusters created by Structure in cies by comparing capture locations to pre- of recently increased connectivity, but a each species are genetically distinct from sumed natal populations, the latter being more detailed consideration of the results one another. Estimates of FST, which is a established by genetic analysis of origins. provides observations on the use of this measure of differences in allele frequen- These movement data for specific individu- habitat linkage by the study species, and cies between populations, were 0.10 for als are qualitatively and functionally com- shows the range and quality of information Cape York Rat and 0.09 for Bush Rat. The parable to the information that one would that genetic data can be expected to pro- estimate of FST based on capture location expect from traditional field methods, like vide. was the same for Cape York Rat, but was telemetry or mark-recapture (Proctor et al. Taken together with the trapping data, considerably lower for Bush Rat (0.04), 2005), and bear little resemblance to ear- our results identified different responses to demonstrating that the Structure clusters lier genetic methods that used biologically the establishment and maturation of rain- more accurately reflected genetic parti- unrealistic models to infer long-term, popu- forest in this linkage. Bush Rats undertook tioning in this species than did capture lation-level estimates of gene flow. many long-distance movements, produced locations. The program of trapping that was similar numbers of colonists from either Marker RfgF6 showed obvious evidence required to collect samples for genetic end, and colonized both ends of the link- of high frequency null alleles in Bush Rat, analysis also produced mark-recapture age (Fig. 3). By contrast, the only Cape with observed heterozygosity (HO; 0.29) data, so the genetic results are of little prac- York Rat (64) that we documented moving falling well below expected heterozygosity tical value unless they provide information into the corridor from Gadgarra subse-
(HE; 0.67). Given the importance of the that could not be obtained directly from quently returned to its natal population. information provided by each marker the field data (ignoring the fact that our This species also failed to produce a single when working with so few markers, and field data could not be used until species capture event in DCGF, whereas its num- given that no individuals appeared to be identifications were confirmed with bers increased steadily through time in homozygous null since we got a strong genetic data; Va´zquez-Domı´nguez et al. DCLB at the other end of the linkage. These genotype for each animal, we opted to 2001). Between the two species, there observations illustrate how knowledge of include this marker in all of our analyses. were six cases where an individual was individual origins could provide informa- Looking across the remaining markers in captured in more than one of the four tion on the habitat conditions or inter-spe- both species, there were no more signifi- areas on which our analysis was based cies interactions that underlie habitat cant heterozygote deficit results (Gene- (Lake Barrine, DCLB,DCGF, Gadgarra). Five suitability and permeability, perhaps lead- pop) than expected due to Type I error. of these were short-distance movements ing to habitat modifications that optimize Intra-population variation differed con- between adjacent areas. By contrast, the linkage function for a target species. siderably by species and location (Table 1). genetic data on individual origins revealed The data also provide insight into the
In both species, HE was higher for the Lake 16 long-distance movements, and con- circumstances that maximized long-dis- Barrine cluster than the Gadgarra cluster, firmed the proximate origin of 25 individu- tance movement in our study system. Six which runs counter to intuition for a forest als that were captured within Donaghy’s of the 16 long-distance movements that we fragment (Lake Barrine) relative to a large Corridor (Figs 2,3). In the single case detected, including the only two such tract of contiguous habitat (Gadgarra). where mark-recapture data detected a movements made by the Cape York Rat,
214 ECOLOGICAL MANAGEMENT & RESTORATION VOL 10 NO 3 DECEMBER 2009 ª 2009 Ecological Society of Australia RESEARCH REPORT occurred in 1998 or earlier, when there relevant to this species. It should be noted, Sumner had the foresight to initiate the col- had only been three individuals from these however, that genetic data were needed to lection of samples for genetic analysis and, species captured within Donaghy’s Corri- resolve the field trap data for this species, while she didn’t have time to take on the dor (Fig. 3). It has been shown that which was occasionally confused with the analysis of those samples, she deserves increasing the width of a linkage can act to Grassland Melomys (M. burtoni). credit for making this project possible. reduce trans-linkage movements, perhaps Both simulation results (Cornuet et al. because the linkage shifts from providing 1999; Paetkau 2004) and case studies et al. References the minimum cover necessary for move- (Manel et al. 2002; Maudet et al. 2002) ment to acting as permanently colonized indicate that the power to assign individu- Andreassen H. P., Halle S. and Ims R. A. (1996) Optimal width of movement corridors for root habitat (Andreassen et al. 1996). We spec- als to a population of origin is relatively voles: not too narrow and not too wide. Jour- ulate that an analogous scenario might low for populations connected by ongoing nal of Applied Ecology 33, 63–70. have operated here, in which movement gene flow, or which have only recently Beier P. and Noss R. F. (1998) Do habitat corridors provide connectivity? Conservation Biology was initially increased as the linkage become separated. Our empirical results 12, 1241–1252. established vegetation cover, but then support the intuition that genetic assign- Berry O., Tocher M. D., Gleeson D. M. and Sarre decreased as the restored habitat matured ment is most effective in the first genera- S. D. (2005) Effect of vegetation matrix on animal dispersal: genetic evidence from a and was colonized. This possibility empha- tions following resumption of movement study of endangered skinks. Conservation sizes the value of beginning sample collec- between populations that had previously Biology 19, 855–864. tion in advance of the habitat modification been demographically isolated from each Cornuet J.-M., Piry S., Luikart G., Estoup A. and Solignac M. (1999) New methods employing that one wishes to monitor. other. One anticipates that the power to multilocus genotypes to select or exclude pop- In addition to being biased in terms of assign origins would decrease over time as ulations as origins of individuals. Genetics when they occurred, the long-distance gene flow reduces genetic differences 153, 1989–2000. Dixon J. D., Oli M. K., Wooten M. C., Eason T. H., movements showed a gender bias, with 13 between populations. McCown J. W. and Paetkau D. (2006) Effec- of 16 movements being undertaken by Although we expect our approach to tiveness of a regional corridor in connecting males. The gender bias in these two spe- be most effective for populations that have two black bear populations. Conservation Biology 20, 155–162. cies was less dramatic amongst the short- experienced several generations of isola- Eldridge M. D. B., Kinnear J. and Onus M. L. distance colonizers, which included 14 tion, the technique also has potential in (2001) Source population of dispersing rock- males and 11 females. longer-lived species, where small effective wallabies. Petrogale lateralis. identified by assignment tests on multilocus genotypic Just as the timing of the long-distance population size would often result in data. Molecular Ecology 10, 2867–2876. dispersal events was noteworthy, it is inter- greater genetic drift per generation (e.g. Falush D., Stephens M. and Pritchard J. K. (2003) esting that the two strongest candidates Dixon et al. 2006). Furthermore, if a Inference of population structure: extensions to linked loci and correlated allele frequencies. for being F1 hybrids (Cape York Rat 504 & substantial amount of habitat is removed Genetics 164, 1567–1587. 613) appeared in the final trapping ses- during a fragmentation event, such that Guinand B., Topchy A., Page K. S., Burnham-Cur- sions of our study (Fig. 3), as expected if genetically intermediate individuals are tis M. K., Punch W. F. and Scribner K. T. (2002) Comparisons of likelihood and machine the linkage had succeeded in re-establish- removed, the remnant populations will learning methods of individual classification. ing gene flow between previously isolated have a degree of genetic separation from Journal of Heredity 93, 260–269. populations. Analysis of extra markers the outset, decreasing the time required to Hinten G., Maguire T., Rossetto M. and Baverstock P. (1999) Isolation and characterization of would confirm the status of these two indi- build up the genetic differences needed for microsatellite loci from the bush rat, Rattus viduals. assigning individual origins. fuscipes greyii. Molecular Ecology 8, 351– We initially targeted three species that We believe that the approach illustrated 352. Laurance W. F. (1994) Rainforest fragmentation we thought might be sensitive to the forest by small mammals in Donaghy’s Corridor and the structure of small mammal communi- fragmentation at our study site, creating a will find many practical applications, help- ties in tropical Queensland. Biological Con- 9-locus microsatellite dataset for 116 Fawn- ing to bridge the gap between population servation 69, 23–32. Manel S., Berthier P. and Luikart G. (2002) Footed Melomys (M. cervinipes). Unfortu- genetics and applied problems in land- Detecting wildlife poaching: identifying the ori- nately this species showed insufficient scape ecology and conservation biology, gin of individuals with Bayesian assignment differentiation across the linkage to allow and providing valuable information on the tests and multilocus genotypes. Conservation Biology 16, 650–659. assignment of individual origins. This spe- function of habitat linkages. Maudet C., Miller C., Bassano B. et al. (2002) cies was also captured in Donaghy’s Corri- Microsatellite DNA and recent statistical dor earlier and more often than the others, methods in wildlife conservation management: Acknowledgements applications in Alpine ibex [Capra ibex. ibex)]. producing as many captures within the Molecular Ecology 11, 421–436. linkage in 1999 and 2000 as in the contigu- This work was supported by the Natural Paetkau D., Calvert W., Stirling I. and Strobeck C. ous forest on either side (not shown). Sciences and Engineering Research Coun- (1995) Microsatellite analysis of population structure in Canadian polar bears. Molecular While biologically interesting, the apparent cil (Canada), the National Council of Ecology 4, 347–354. reduced sensitivity of Fawn-Footed Melo- Science and Technology (Mexico), the Aus- Paetkau D., Slade R., Buden M. and Estoup A. mys to this segment of unforested habitat tralian Research Council and the Queens- (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: meant that our study methods were not land Department of Environment. Jo
ª 2009 Ecological Society of Australia ECOLOGICAL MANAGEMENT & RESTORATION VOL 10 NO 3 DECEMBER 2009 215 RESEARCH REPORT
a simulation-based exploration of accuracy exact tests and ecumenicism. Journal of Tucker N. I. J. and Simmons T. (2009) Restoring a and power. Molecular Ecology 13, 55–66. Heredity 86, 248–249. rainforest habitat linkage in north Queensland: Piry S., Alapetite A., Cornuet J.-M., Paetkau D., Roques S., Duchesne P. and Bernatchez L. (1999) Donaghy’s Corridor. Ecological Management Baudouin L. and Estoup A. (2004) GeneClass Potential of microsatellites for individual & Restoration 10, 98–112. 2: an assignment software to select or exclude assignment: the North Atlantic redfish (genus Va´zquez-Domı´nguez E., Paetkau D., Tucker N., populations as origins of individuals. The Jour- Sebastes) species complex as a case study. Hinten G. and Moritz C. (2001) Resolution of nal of Heredity 95, 536–539. Molecular Ecology 8, 1703–1717. natural groups using iterative assignment Primmer C. R., Aho T., Piironen J., Estoup A., Rosenberg D. K., Noon B. R. and Meslow C. tests: an example from two species of Austra- Cornuet J.-M. and Ranta E. (1999) Microsat- (1997) Biological corridors: form, function and lian native rats. (Rattus). Molecular Ecology ellite analysis of hatchery stocks and natural efficacy. BioScience 47, 677–687. 10, 2069–2078. populations of Arctic char, Salvelinus alpinus, Simberloff D., Farr J. A., Cox J. and Mehlman D. Wahlund S. (1928) Zusammensetzung von popula- from the Nordic region: implications for con- W. (1992) Movement corridors: conservation tionen und korrelationserscheinungen vom servation. Hereditas 130, 277–289. bargains or poor investments? Conservation standpunkt der vererbungslehre aus betrach- Pritchard J. K., Stephens M. and Donnelly P.(2000) Biology 6, 493–504. tet. Hereditas 11, 65–106. Inference of population structure using multilo- Tewksbury J. J., Levey D. J., Haddad N. M. et al. Wiens J. A. (1997) Metapopulation dynamics and cus genotype data. Genetics 155, 945–959. (2002) Corridors affect plants, animals, and landscape ecology. In: Metapopulation Biology Proctor M., McLellan B. N., Barclay R. M. R. and their interactions in fragmented landscapes. (eds I. A. Hanski and M. E. Gilpin) pp. 43–62. Strobeck C. (2005) Genetic analysis reveals Proceedings of the National Academy of Sci- Academic Press, San Diego. demographic fragmentation of grizzly bears ences of the USA 99, 12923–12926. Williams S. E., Marsh H. and Winter J. (2002) Spa- yielding vulnerably small populations. Pro- Tucker N. I. J. (2000a) Linkage restoration: inter- tial scale, species diversity, and habitat struc- ceedings of the Royal Society B: Biological preting fragmentation theory for the design of ture: small mammals in Australian tropical rain Sciences 272, 2409–2416. a rainforest linkage in the humid wet tropics of forest. Ecology 83, 1317–1329. Rannala B. and Mountain J. L. (1997) Detecting north-eastern Queensland. Ecological Man- Wright S. (1951) The genetical structure of popu- immigration by using multilocus genotypes. agement & Restoration 1, 35–41. lations. Eugenics 15, 323–354. Proceedings of the National Academy of Sci- Tucker N. I. J. (2000b) Evaluating effectiveness of ences of the USA 94, 9197–9201. restored habitat linkages at Donaghy’s corri- Raymond M. and Rousset F. (1995) GENEPOP dor: measures used and questions asked. Eco- (Version 1.2): population genetics software for logical Management & Restoration 1, 61–62.
216 ECOLOGICAL MANAGEMENT & RESTORATION VOL 10 NO 3 DECEMBER 2009 ª 2009 Ecological Society of Australia