Mark D. B. Eldridge

Assessing the benefits and risks of translocations in changing environments: a genetic perspective

Translocations are being increasingly proposed as a way of conserving biodiversity, particularly in the management of threatened and keystone species, with the aims of maintaining biodiversity and ecosystem function under the combined pressures of habitat fragmentation and climate change. Evolutionary genetic considerations should be an important part of translocation strategies, but there is often confusion about concepts and goals. Here, we provide a classification of translocations based on specific genetic goals for both threatened species and ecological restoration, separating targets based on ‘genetic rescue’ of current population fitness from those focused on maintaining adaptive potential. We then provide a framework for assessing the genetic benefits and risks associated with translocations and provide guidelines for managers focused on conserving biodiversity and evolutionary processes. Case studies are developed to illustrate the framework.

Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial

A fatal transmissible tumor spread between individuals by biting has emerged in the Tasmanian devil (Sarcophilus harrisii), a carnivorous marsupial. Here we provide genetic evidence establishing that the tumor is clonal and therefore foreign to host devils. Thus, the disease is highly unusual because it is not just a tumor but also a tissue graft, passed between individuals without invoking an immune response. The MHC plays a key role in immune responses to both tumors and grafts. The most common mechanism of immune evasion by tumors is down-regulation of classical cell surface MHC molecules. Here we show that this mode of immune escape does not occur. However, because the tumor is a graft, it should still be recognized and rejected by the hosts immune system due to foreign cell surface antigens. Mixed lymphocyte responses showed a lack of alloreactivity between lymphocytes of different individuals in the affected population, indicating a paucity of MHC diversity. This result was verified by genotyping, providing a conclusive link between a loss of MHC diversity and spread of a disease through a wild population. This novel disease arose as a direct result of loss of genetic diversity and the aggressive behavior of the host species. The neoplastic clone continues to spread although the population, and, without active disease control by removal of affected animals and the isolation of disease-free animals, the Tasmanian devil faces extinction.

Source population of dispersing rock‐wallabies (Petrogale lateralis) idengified by assignment tests on multilocus genotypic data

The ability to confidently idengify or exclude a population as the source of an individual has numerous powerful applications in molecular ecology. Several alternative assignment methods have recently been developed and are yet to be fully evaluated with empirical data. In this study we tested the efficacy of different assignment methods by using a translocated rock‐wallaby (Petrogale lateralis) population, of known provenance. Specimens from the translocated population (n = 43), its known source population (n = 30) and four other nearby populations (n = 19–32) were genotyped for 11 polymorphic microsatellite loci. The results idengified Bayesian clustering, frequency and Bayesian methods as the most consistent and accurate, correctly assigning 93–100% of individuals up to a significance threshold of P = 0.01. Performance was variable among the distance‐based methods, with the Cavalli‐Sforza and Edwards chord distance performing best, whereas Goldstein et al.’s (δµ)2 consistently performed poorly. Using Bayesian clustering, frequency and Bayesian methods we then attempted to determine the source of rock‐wallabies which have recently recolonized an outcrop (Gardners) 8 km from the nearest rock‐wallaby population. Results indicate that the population at Gardners originated via a recent dispersal event from the eastern end of Mt. Caroline. This is only the second published record of dispersal by rock‐wallabies between habitat patches and is the longest movement recorded to date. Molecular techniques and methods of analysis are now available to allow detailed studies of dispersal in rock‐wallabies and should also be possible for many other taxa.

Genomic Instability within Centromeres of Interspecific Marsupial Hybrids

Several lines of evidence suggest that, within a lineage, particular genomic regions are subject to instability that can lead to specific types of chromosome rearrangements important in species incompatibility. Within family Macropodidae (kangaroos, wallabies, bettongs, and potoroos), which exhibit recent and extensive karyotypic evolution, rearrangements involve chiefly the centromere. We propose that centromeres are the primary target for destabilization in cases of genomic instability, such as interspecific hybridization, and participate in the formation of novel chromosome rearrangements. Here we use standard cytological staining, cross-species chromosome painting, DNA probe analyses, and scanning electron microscopy to examine four interspecific macropodid hybrids (Macropus rufogriseus × Macropus agilis). The parental complements share the same centric fusions relative to the presumed macropodid ancestral karyotype, but can be differentiated on the basis of heterochromatic content, M. rufogriseus having larger centromeres with large C-banding positive regions. All hybrids exhibited the same pattern of chromosomal instability and remodeling specifically within the centromeres derived from the maternal (M. rufogriseus) complement. This instability included amplification of a satellite repeat and a transposable element, changes in chromatin structure, and de novo whole-arm rearrangements. We discuss possible reasons and mechanisms for the centromeric instability and remodeling observed in all four macropodid hybrids.

Genetic diversity in remnant mainland and "pristine"’ island populations of three endemic Australian macropodids (Marsupialia): Macropus eugenii, Lagorchestes hirsutus and Petrogale lateralis

Since European settlement, mainland Australia has experienced a wave of mammal extinctions and population declines. However, some species have persisted on off-shore islands, which are now viewed as important wildlife refuges. In this study, we assessed the level of genetic diversity, at 7–11 microsatellite loci, in island and remnant mainland populations of three endemic species of macropodid marsupial; the tammar wallaby Macropus eugenii(n = 92); rufous hare-wallaby Lagorchestes hirsutus(n = 40) and black-footed rock-wallaby Petrogale lateralis(n = 164). There was a consistent pattern of significantly higher levels of microsatellite diversity in the remnant mainland population (A= 4.9–13.9; He= 0.61–0.86) of each species compared to conspecific “pristine” island populations (A= 1.2–3.7; He= 0.05–0.44). These marked differences are even apparent where island populations currently have a substantially larger census size. In addition, island populations were substantially inbred (Fe= 0.49–0.91). Although island populations have been insulated from the relatively recent threatening processes operating on the mainland, they have nevertheless been significantly impacted by increased inbreeding and the substantial erosion of genetic diversity. Despite the difficulties of ensuring the survival of remnant mainland populations, they appear to retain substantially more genetic diversity than their island counterparts and therefore are more likely to contribute to the long-term persistence of their species. These data also demonstrate that small remnant mainland populations (n < 10–20) are often capable of rapid recovery and are not necessarily genetically depauperate.

Multifaceted genetic analysis of the "Critically Endangered" brush-tailed rock-wallaby Petrogale penicillata in Victoria, Australia: implications for management

The use of molecular genetic techniques can aidwildlife managers in setting priorities anddevising management strategies for scatteredpopulations of threatened taxa. In this study,six remnant populations of the “criticallyendangered” brush-tailed rock-wallaby (Petrogale penicillata) in Victoria, Australia,were examined using karyotypic, microsatellite(11 loci) and mitochondrial DNA (mtDNA) controlregion sequence analysis. Each remnantpopulation was found to be genetically distinct(unique microsatellite alleles and controlregion haplotypes), but had low geneticdiversity. This distribution of geneticdiversity between, rather than withinpopulations, is most likely a consequence ofrecent severe reductions in population size anddispersal that have occurred since Europeansettlement. The six mtDNA control regionhaplotypes identified in the Victorianpopulations were all closely related (average1.3% sequence divergence), and only 2%divergence separated haplotypes from EastGippsland and the Grampians (550 km to thewest). In contrast there was considerablesequence divergence (7.7%) between theVictorian haplotypes and those found in P.penicillata from elsewhere in the speciesrange. In comparison, 8.8% divergenceseparates P. penicillata from the closelyrelated P. herberti. The Victorianhaplotypes also formed a distinct and wellsupported monophyletic group that excludedhaplotypes from other P. penicillata andP. herberti. In light of these data, werecommend that the remnant Victorianpopulations of P. penicillata be managedseparately from remaining populations in NewSouth Wales and Queensland; and thatindividuals be regularly exchanged amongst theVictorian populations to increase theirdiversity and reduce the likelihood ofinbreeding depression.

Multiple biogeographical barriers identified across the monsoon tropics of northern Australia: Phylogeographic analysis of the brachyotis group of rock-wallabies

The monsoon tropics of northern Australia are a globally significant biodiversity hotspot, but its phylogeography is poorly known. A major challenge for this region is to understand the biogeographical processes that have shaped the distribution and diversity of taxa, without detailed knowledge of past climatic and environmental fluctuations. Although molecular data have great potential to address these questions, only a few species have been examined phylogeographically. Here, we use the widely distributed and abundant short‐eared rock‐wallaby (Petrogale brachyotis; n = 101), together with the sympatric monjon (P. burbidgei; n = 11) and nabarlek (P. concinna; n = 1), to assess historical evolutionary and biogeographical processes in northern Australia. We sequenced ∼1000 bp of mitochondrial DNA (control region, ND2) and ∼3000 bp of nDNA (BRCA1, ω‐globin and two anonymous loci) to investigate phylogeographic structuring and delineate the time‐scale of diversification within the region. Our results indicate multiple barriers between the Top End (Northern Territory) and Kimberley (Western Australia), which have caused divergence throughout the Plio‐Pleistocene. Eight geographically discrete and genetically distinct lineages within the brachyotis group were identified, five of which are separated by major river valleys (Ord, Victoria, Daly), arid lowlands and discontinuous sandstone ranges. It is likely that these barriers have similarly influenced genetic structure in other monsoonal biota.

Landscape discontinuities influence gene flow and genetic structure in a large, vagile Australian mammal, Macropus fuliginosus

Large vagile mammals typically exhibit little genetic structuring across their range, particularly when their habitat is essentially continuous. We investigated the population genetic structure of a large vagile Australian macropodid, Macropus fuliginosus, which is continuously distributed across most of southern Australia, using nine highly polymorphic nuclear microsatellite loci. Five distinct genetic units were identified across the range, four on the mainland and one on Kangaroo Island. In addition to the predicted historic Nullarbor Plain Barrier, two unexpected mainland barriers to gene flow were identified. Both were associated with landscape discontinuities (Swan River, Flinders Ranges), which appear within the dispersal capabilities of M. fuliginosus. Typical of large vagile mammals, M. fuliginosus displays high genetic diversity (with the exception of an insular population) and weak genetic structuring (within genetic units). However, the expansion of M. fuliginosus from southwestern Australia during the Pleistocene has resulted in significantly reduced genetic diversity in eastern populations. No significant sex‐biased dispersal was detected, although differences in habitat, densities and climatic conditions between the eastern and western regions of the range appear to influence dispersal with the effects of isolation by distance only evident in the west. These results suggest that the biogeography of southern Australia is more complex than previously thought and reveal that seemingly minor landscape features can significantly impact genetic structuring in large vagile mammals.

Microsatellite variation and population structure in a declining Australian Hylid Litoria aurea

The green and golden bell frog (Litoria aurea) was once a common Australian Hylid. Today, many populations are small and fragmented as a result of dramatic declines in distribution and abundance. We undertook a large‐scale assessment of genetic structure and diversity in L. aurea using four species‐specific microsatellite markers. Twenty‐one locations were sampled from throughout the species range covering 1000 km of the east coast of Australia. Levels of allelic diversity and heterozygosity were high (uncorrected mean alleles/locus and HE were 4.8–8.8 and 0.43–0.8, respectively) compared to other amphibian species and significant differences among sampled sites were recorded. Despite recent population declines, no sites displayed a genetic signature indicative of a population bottleneck. Significant genetic structuring (overall FST 0.172) was detected throughout the species range, but was relatively low compared to previous amphibian studies employing microsatellites. In addition we found that some areas sampled within continuous habitat showed evidence of weak genetic structuring (data subset FST 0.034). We conclude that maintaining areas of continuous habitat is critical to the conservation of the species and argue that population recovery and/or persistence in all areas sampled is possible if appropriate protection and management are afforded.

Radiation of chromosome shuffles

Rock wallabies, Petrogale, exhibit chromosome diversity that is exceptional in marsupials, with 20 distinct chromosome races being recognized. Many of the karyotypic changes identified within Petrogale appear to be recent, although the rate of chromosome evolution varies between taxa. While the patchy distribution of Petrogale and their social structure would facilitate the fixation of novel rearrangements, these factors alone do not explain the pattern of chromosome evolution shown in this group. The chromosome changes that have come to characterize each taxon may offer selective advantages in the particular areas occupied, or it may be that these rearrangements play an important role in reproductive isolation. In Petrogale, the taxa with the largest number of chromosome rearrangements are those that are sympatric, or have multiple zones of parapatry, with other members of the genus. Male hybrids from a variety of chromosomal admixtures were found to be sterile, but with those heterozygous for the least complex rearrangements being least affected. As expected, equivalent female hybrids were less severely affected. Chromosomal and genic changes both appear important in these processes.