Marsupial Genetics and Genomics

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Animal Genetics and Genomics".

Deadline for manuscript submissions: closed (31 August 2019) | Viewed by 32913

Special Issue Editors


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Guest Editor
Institute for Applied Ecology, University of Canberra, Canberra, Australia
Interests: cytogenetic; epigenoimics tracing the evolution of amniote chromosomes

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Guest Editor
Research School of Biology and The John Curtin School of Medical Research, Australian National University, Canberra, Australia
Interests: conservation genetics; phylogenomics; comparative genomics; evolution; sequencing

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Guest Editor
Australian Museum Research Institute, Australian Museum, Sydney, Australia

Special Issue Information

Dear Colleagues,

Marsupials are fascinating animals, giving birth to tiny, altricial young that typically spend the first part of their life developing in their mother’s pouch. Since the sequencing of the first marsupial genome over a decade ago, genomics has helped to uncover the evolutionary origins of some of the unique features of marsupials. There are over 300 marsupial species distributed between the Americas and Australasia, but many of these are listed as threatened species, especially in Australia. There is now a concerted effort to more fully utilise genomics to understand the evolution of and phylogenetic relationships among Australian marsupials, and contribute directly to their conservation management, through the Oz Mammals Genomics Initiative. Such studies are informing management decisions and captive breeding programs, and providing insight into the evolutionary origin of marsupial features.
In this Special Issue, we aim to highlight the areas where marsupial genetics and genomics studies have had an impact on our understanding of marsupial biology or conservation. We invite submissions of either review or original research articles on any aspect of marsupial genetics and genomics, but we especially welcome submissions detailing the use of recently developed technologies. 

Dr. Janine Deakin
Dr. Anna MacDonald
Dr. Mark Eldridge
Guest Editors

Manuscript Submission Information

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Keywords

  • conservation genetics
  • phylogenomics
  • comparative genomics
  • evolution
  • sequencing

Published Papers (8 papers)

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Research

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21 pages, 4046 KiB  
Article
Multi-Species Phylogeography of Arid-Zone Sminthopsinae (Marsupialia: Dasyuridae) Reveals Evidence of Refugia and Population Expansion in Response to Quaternary Change
by Linette S. Umbrello, Raphael K. Didham, Ric A. How and Joel A. Huey
Genes 2020, 11(9), 963; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11090963 - 20 Aug 2020
Cited by 10 | Viewed by 3415
Abstract
Historical population contraction and expansion events associated with Pleistocene climate change are important drivers of intraspecific population structure in Australian arid-zone species. We compared phylogeographic patterns among arid-adapted Dasyuridae (Sminthopsis and Planigale) with close phylogenetic relationships and similar ecological roles to [...] Read more.
Historical population contraction and expansion events associated with Pleistocene climate change are important drivers of intraspecific population structure in Australian arid-zone species. We compared phylogeographic patterns among arid-adapted Dasyuridae (Sminthopsis and Planigale) with close phylogenetic relationships and similar ecological roles to investigate the drivers of phylogeographic structuring and the importance of historical refugia. We generated haplotype networks for two mitochondrial (control region and cytochrome b) and one nuclear (omega-globin) gene from samples distributed across each species range. We used ΦST to test for a genetic population structure associated with the four Pilbara subregions, and we used expansion statistics and Bayesian coalescent skyline analysis to test for signals of historical population expansion and the timing of such events. Significant population structure associated with the Pilbara and subregions was detected in the mitochondrial data for most species, but not with the nuclear data. Evidence of population expansion was detected for all species, and it likely began during the mid-late Pleistocene. The timing of population expansion suggests that these species responded favorably to the increased availability of arid habitats during the mid-late Pleistocene, which is when previously patchy habitats became more widespread. We interpret our results to indicate that the Pilbara region could have acted as a refugium for small dasyurids. Full article
(This article belongs to the Special Issue Marsupial Genetics and Genomics)
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17 pages, 4443 KiB  
Article
Comparative Cytogenetic Mapping and Telomere Analysis Provide Evolutionary Predictions for Devil Facial Tumour 2
by Emory D. Ingles and Janine E. Deakin
Genes 2020, 11(5), 480; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11050480 - 28 Apr 2020
Cited by 1 | Viewed by 2505
Abstract
The emergence of a second transmissible tumour in the Tasmanian devil population, devil facial tumour 2 (DFT2), has prompted questions on the origin and evolution of these transmissible tumours. We used a combination of cytogenetic mapping and telomere length measurements to predict the [...] Read more.
The emergence of a second transmissible tumour in the Tasmanian devil population, devil facial tumour 2 (DFT2), has prompted questions on the origin and evolution of these transmissible tumours. We used a combination of cytogenetic mapping and telomere length measurements to predict the evolutionary trajectory of chromosome rearrangements in DFT2. Gene mapping by fluorescence in situ hybridization (FISH) provided insight into the chromosome rearrangements in DFT2 and identified the evolution of two distinct DFT2 lineages. A comparison of devil facial tumour 1 (DFT1) and DFT2 chromosome rearrangements indicated that both started with the fusion of a chromosome, with potentially critically short telomeres, to chromosome 1 to form dicentric chromosomes. In DFT1, the dicentric chromosome resulted in breakage–fusion–bridge cycles leading to highly rearranged chromosomes. In contrast, the silencing of a centromere on the dicentric chromosome in DFT2 stabilized the chromosome, resulting in a less rearranged karyotype than DFT1. DFT2 retains a bimodal distribution of telomere length dimorphism observed on Tasmanian devil chromosomes, a feature lost in DFT1. Using long term cell culture, we observed homogenization of telomere length over time. We predict a similar homogenization of telomere lengths occurred in DFT1, and that DFT2 is unlikely to undergo further substantial rearrangements due to maintained telomere length. Full article
(This article belongs to the Special Issue Marsupial Genetics and Genomics)
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24 pages, 2665 KiB  
Article
Understanding Historical Demographic Processes to Inform Contemporary Conservation of an Arid Zone Specialist: The Yellow-Footed Rock-Wallaby
by Sally Potter, Linda E. Neaves, Mark Lethbridge and Mark D. B. Eldridge
Genes 2020, 11(2), 154; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11020154 - 31 Jan 2020
Cited by 2 | Viewed by 3113
Abstract
Little genetic research has been undertaken on mammals across the vast expanse of the arid biome in Australia, despite continuing species decline and need for conservation management. Here, we evaluate the contemporary and historical genetic connectivity of the yellow-footed rock-wallaby, Petrogale xanthopus xanthopus [...] Read more.
Little genetic research has been undertaken on mammals across the vast expanse of the arid biome in Australia, despite continuing species decline and need for conservation management. Here, we evaluate the contemporary and historical genetic connectivity of the yellow-footed rock-wallaby, Petrogale xanthopus xanthopus, a threatened macropodid which inhabits rocky outcrops across the disconnected mountain range systems of the southern arid biome. We use 17 microsatellite loci together with mitochondrial control region data to determine the genetic diversity of populations and the evolutionary processes shaping contemporary population dynamics on which to base conservation recommendations. Our results indicate the highly fragmented populations have reduced diversity and limited contemporary gene flow, with most populations having been through population bottlenecks. Despite limited contemporary gene flow, the phylogeographic relationships of the mitochondrial control region indicate a lack of structure and suggests greater historical connectivity. This is an emerging outcome for mammals across this arid region. On the basis of our results, we recommend augmentation of populations of P. x. xanthopus, mixing populations from disjunct mountain range systems to reduce the chance of continued diversity loss and inbreeding depression, and therefore maximize the potential for populations to adapt and survive into the future. Full article
(This article belongs to the Special Issue Marsupial Genetics and Genomics)
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20 pages, 1527 KiB  
Article
Population Genomics of Bettongia lesueur: Admixing Increases Genetic Diversity with no Evidence of Outbreeding Depression
by Kate Rick, Kym Ottewell, Cheryl Lohr, Rujiporn Thavornkanlapachai, Margaret Byrne and W. Jason Kennington
Genes 2019, 10(11), 851; https://0-doi-org.brum.beds.ac.uk/10.3390/genes10110851 - 28 Oct 2019
Cited by 19 | Viewed by 4147
Abstract
Small and isolated populations are subject to the loss of genetic variation as a consequence of inbreeding and genetic drift, which in turn, can affect the fitness and long-term viability of populations. Translocations can be used as an effective conservation tool to combat [...] Read more.
Small and isolated populations are subject to the loss of genetic variation as a consequence of inbreeding and genetic drift, which in turn, can affect the fitness and long-term viability of populations. Translocations can be used as an effective conservation tool to combat this loss of genetic diversity through establishing new populations of threatened species, and to increase total population size. Releasing animals from multiple genetically diverged sources is one method to optimize genetic diversity in translocated populations. However, admixture as a conservation tool is rarely utilized due to the risks of outbreeding depression. Using high-resolution genomic markers through double-digest restriction site-associated sequencing (ddRAD-seq) and life history data collected over nine years of monitoring, this study investigates the genetic and fitness consequences of admixing two genetically-distinct subspecies of Bettongia lesueur in a conservation translocation. Using single nucleotide polymorphisms (SNPs) identified from 215 individuals from multiple generations, we found an almost 2-fold increase in genetic diversity in the admixed translocation population compared to the founder populations, and this was maintained over time. Furthermore, hybrid class did not significantly impact on survivorship or the recruitment rate and therefore we found no indication of outbreeding depression. This study demonstrates the beneficial application of mixing multiple source populations in the conservation of threatened species for minimizing inbreeding and enhancing adaptive potential and overall fitness. Full article
(This article belongs to the Special Issue Marsupial Genetics and Genomics)
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15 pages, 2483 KiB  
Article
Transcriptomics of Tasmanian Devil (Sarcophilus Harrisii) Ear Tissue Reveals Homogeneous Gene Expression Patterns across a Heterogeneous Landscape
by Alexandra K. Fraik, Corey Quackenbush, Mark J. Margres, Sebastien Comte, David G. Hamilton, Christopher P. Kozakiewicz, Menna Jones, Rodrigo Hamede, Paul A. Hohenlohe, Andrew Storfer and Joanna L. Kelley
Genes 2019, 10(10), 801; https://0-doi-org.brum.beds.ac.uk/10.3390/genes10100801 - 12 Oct 2019
Cited by 6 | Viewed by 5076
Abstract
In an era of unprecedented global change, exploring patterns of gene expression among wild populations across their geographic range is crucial for characterizing adaptive potential. RNA-sequencing studies have successfully characterized gene expression differences among populations experiencing divergent environmental conditions in a wide variety [...] Read more.
In an era of unprecedented global change, exploring patterns of gene expression among wild populations across their geographic range is crucial for characterizing adaptive potential. RNA-sequencing studies have successfully characterized gene expression differences among populations experiencing divergent environmental conditions in a wide variety of taxa. However, few of these studies have identified transcriptomic signatures to multivariate, environmental stimuli among populations in their natural environments. Herein, we aim to identify environmental and sex-driven patterns of gene expression in the Tasmanian devil (Sarcophilus harrisii), a critically endangered species that occupies a heterogeneous environment. We performed RNA-sequencing on ear tissue biopsies from adult male and female devils from three populations at the extremes of their geographic range. There were no transcriptome-wide patterns of differential gene expression that would be suggestive of significant, environmentally-driven transcriptomic responses. The general lack of transcriptome-wide variation in gene expression levels across the devil’s geographic range is consistent with previous studies that documented low levels of genetic variation in the species. However, genes previously implicated in local adaptation to abiotic environment in devils were enriched for differentially expressed genes. Additionally, three modules of co-expressed genes were significantly associated with either population of origin or sex. Full article
(This article belongs to the Special Issue Marsupial Genetics and Genomics)
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18 pages, 1885 KiB  
Article
Mixing Genetically and Morphologically Distinct Populations in Translocations: Asymmetrical Introgression in A Newly Established Population of the Boodie (Bettongia lesueur)
by Rujiporn Thavornkanlapachai, Harriet R. Mills, Kym Ottewell, Judy Dunlop, Colleen Sims, Keith Morris, Felicity Donaldson and W. Jason Kennington
Genes 2019, 10(9), 729; https://0-doi-org.brum.beds.ac.uk/10.3390/genes10090729 - 19 Sep 2019
Cited by 21 | Viewed by 3232
Abstract
The use of multiple source populations provides a way to maximise genetic variation and reduce the impacts of inbreeding depression in newly established translocated populations. However, there is a risk that individuals from different source populations will not interbreed, leading to population structure [...] Read more.
The use of multiple source populations provides a way to maximise genetic variation and reduce the impacts of inbreeding depression in newly established translocated populations. However, there is a risk that individuals from different source populations will not interbreed, leading to population structure and smaller effective population sizes than expected. Here, we investigate the genetic consequences of mixing two isolated, morphologically distinct island populations of boodies (Bettongia lesueur) in a translocation to mainland Australia over three generations. Using 18 microsatellite loci and the mitochondrial D-loop region, we monitored the released animals and their offspring between 2010 and 2013. Despite high levels of divergence between the two source populations (FST = 0.42 and ϕST = 0.72), there was clear evidence of interbreeding between animals from different populations. However, interbreeding was non-random, with a significant bias towards crosses between the genetically smaller-sized Barrow Island males and the larger-sized Dorre Island females. This pattern of introgression was opposite to the expectation that male–male competition or female mate choice would favour larger males. This study shows how mixing diverged populations can bolster genetic variation in newly established mammal populations, but the ultimate outcome can be difficult to predict, highlighting the need for continued genetic monitoring to assess the long-term impacts of admixture. Full article
(This article belongs to the Special Issue Marsupial Genetics and Genomics)
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Review

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14 pages, 3234 KiB  
Review
Hormonal and Molecular Regulation of Phallus Differentiation in a Marsupial Tammar Wallaby
by Yu Chen and Marilyn B. Renfree
Genes 2020, 11(1), 106; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11010106 - 16 Jan 2020
Viewed by 3277
Abstract
Congenital anomalies in phalluses caused by endocrine disruptors have gained a great deal of attention due to its annual increasing rate in males. However, the endocrine-driven molecular regulatory mechanism of abnormal phallus development is complex and remains largely unknown. Here, we review the [...] Read more.
Congenital anomalies in phalluses caused by endocrine disruptors have gained a great deal of attention due to its annual increasing rate in males. However, the endocrine-driven molecular regulatory mechanism of abnormal phallus development is complex and remains largely unknown. Here, we review the direct effect of androgen and oestrogen on molecular regulation in phalluses using the marsupial tammar wallaby, whose phallus differentiation occurs after birth. We summarize and discuss the molecular mechanisms underlying phallus differentiation mediated by sonic hedgehog (SHH) at day 50 pp and phallus elongation mediated by insulin-like growth factor 1 (IGF1) and insulin-like growth factor binding protein 3 (IGFBP3), as well as multiple phallus-regulating genes expressed after day 50 pp. We also identify hormone-responsive long non-coding RNAs (lncRNAs) that are co-expressed with their neighboring coding genes. We show that the activation of SHH and IGF1, mediated by balanced androgen receptor (AR) and estrogen receptor 1 (ESR1) signalling, initiates a complex regulatory network in males to constrain the timing of phallus differentiation and to activate the downstream genes that maintain urethral closure and phallus elongation at later stages. Full article
(This article belongs to the Special Issue Marsupial Genetics and Genomics)
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17 pages, 327 KiB  
Review
The Value of Reference Genomes in the Conservation of Threatened Species
by Parice Brandies, Emma Peel, Carolyn J. Hogg and Katherine Belov
Genes 2019, 10(11), 846; https://0-doi-org.brum.beds.ac.uk/10.3390/genes10110846 - 25 Oct 2019
Cited by 65 | Viewed by 7421
Abstract
Conservation initiatives are now more crucial than ever—over a million plant and animal species are at risk of extinction over the coming decades. The genetic management of threatened species held in insurance programs is recommended; however, few are taking advantage of the full [...] Read more.
Conservation initiatives are now more crucial than ever—over a million plant and animal species are at risk of extinction over the coming decades. The genetic management of threatened species held in insurance programs is recommended; however, few are taking advantage of the full range of genomic technologies available today. Less than 1% of the 13505 species currently listed as threated by the International Union for Conservation of Nature (IUCN) have a published genome. While there has been much discussion in the literature about the importance of genomics for conservation, there are limited examples of how having a reference genome has changed conservation management practice. The Tasmanian devil (Sarcophilus harrisii), is an endangered Australian marsupial, threatened by an infectious clonal cancer devil facial tumor disease (DFTD). Populations have declined by 80% since the disease was first recorded in 1996. A reference genome for this species was published in 2012 and has been crucial for understanding DFTD and the management of the species in the wild. Here we use the Tasmanian devil as an example of how a reference genome has influenced management actions in the conservation of a species. Full article
(This article belongs to the Special Issue Marsupial Genetics and Genomics)
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