Genetic Rescue of Australian Wildlife
ARC Linkage Project LP160100482 2017-2023
Investigators listed on Australian Research Council award: Paul Sunnucks and Sasha Pavlova (Monash U), John Morgan (La Trobe U), Mark Lintermans (U Canberra), Steve Sinclair (DELWP), Michael Magrath (ZoosVic), Andrzej Killian (DArT), David Coates (DBCA), Andrew Young (CSIRO), Matthew Beitzel (ACT Gov.)
PhD students: Joe Zilko (Leadbeater’s possum), Maiko Lutz (Macquarie perch), Yael Rodger (button wrinklewort: grassland daisy), Diana Robledo-Ruiz (Helmeted Honeyeater).
Former honours student: Sara Petrovic (Helmeted Honeyeater)
Contributors: Dan Harley, Zeb Tonkin, Jo Kearns, Bruce Quin, Katherine Harrisson, Brett Ingram, Jarod Lyon, Kim Miller, Neil Murray, Karina Cartwright, Margaret Byrne, Laura Hurley, Helen Taylor, Peter Menkhorst and many others!
Universities: Monash University, La Trobe University
Linkage project Partner Organizations: Victorian Department of Environment, Land, Water and Planning (DELWP), Diversity Arrays Technology, Zoos Victoria, Environment, Planning & Sustainable Development Directorate (ACT Government), Department of Parks and Wildlife (Western Australia) (now Department of Biodiversity, Conservation and Attractions), University of Canberra
Overview: As a result of human landscape modifications, populations of plants and animals around the world are subject to genetic deterioration through isolation into small populations. Without intervention, many of these populations will become extinct, with important contributors being genetic issues such as inbreeding depression and loss of adaptive potential. Genetic rescue – augmented gene flow in populations suffering genetic problems – is one of the most promising interventions for reversing these declines.
Aims: This project aims to evaluate genetic rescue as an effective and efficient recovery technique for threatened populations by applying it to five Critically Endangered/Endangered species of plants and animals. The project will determine whether gene flow will increase the persistence of their populations.
This main aim will be approached by:
Identifying populations needing genetic rescue, and potential donor populations
Conducting a risk assessment for outbreeding depression (loss of fitness when populations that are too different are crossed)
Designing genetic rescue in captive and/or field populations
Implementing experimental genetic rescue, and monitoring the fitness and genomic responses
Making recommendations to guide future applications of genetic rescue
The five target species are:
Photo credits: BW Steve Sinclair, FLB Dave Coates, MP Gunther Schmida, HeHo Peter Menkhorst, LBP Dan Harley
For an overview of these projects, see this short, illustrated Scientia article
Button Wrinklewort: this species of endangered grassland daisy has been reduced from common and widespread to disjunct, mostly small populations in Victoria and the Australian Capital Territory (ACT). There is only a single remaining substantial Victorian diploid population, and a few more in the ACT and New South Wales. The Button Wrinklewort is self-incompatible (individuals cannot mate readily with themselves or close relatives), based on an ‘SI’ gene. Small populations lose SI alleles, so become limited for suitable mates. Small Victorian populations require genetic management, and are being outcrossed among each other, and ACT individuals. Greenhouse controlled-crosses of varying divergence have been be planted into the field, and are being monitored for viability and fecundity (fitness) traits as well as changes in their genomes. Yael Rodger is analysing genomic data to plan genetic management of diploid and tetraploid populations, and recommendations are being implemented specieswide (Rodger et al. 2021).
Below is a graphic summary of some key points about this project. The people whose names are circled in red are key collaborators from management agencies with whom we co-design practical genetic rescue and its science.
Feather-leaved Banksia is self-compatible. It has been reduced to <20 mostly tiny populations in three disjunct areas. There have been two experimental reintroductions: (1) seedlings from 3 extinct populations from one region, (2) seedlings from 2 extinct populations from another. The fitness and genomic effects of crossing are being monitored.
Leadbeater’s Possum: Limited to a single large isolated population in Victoria in montane forest and sub-alpine woodland, and the distinct, small and strongly declining Yellingbo population in lowland swamp forest. We conducted genetic risk assessment to plan future gene flow (Zilko et al. 2020, 2021). Crosses are being attempted in captivity and the wild between lowland and highland Leadbeater's possums. Crosses will be monitored for viability and fecundity fitness traits. Population monitoring of Leadbeater’s Possums at Yellingbo has been as comprehensive as for any Australian mammal, enabling a very rare assessment of the negative effects of inbreeding over an individuals' lifetimes (Zilko et al. 2020). The project has produced a high-quality genome, to help analyse a broad array of genomic data.
Below is a graphic summary of some key points about this project. The people whose names are circled in red are key collaborators from management agencies with whom we co-design practical genetic rescue and its science.
Macquarie Perch: This species has contracted into isolated headwaters that are mostly not likely to be self-sustaining. Populations that are much more similar to those before human impacts in the last 200 years could be recreated by admixture of multiple fragments. In Victoria, admixed offspring from sampled parents have been released in to the Ovens River. These are being monitored for fitness and genomic consequences of admixture, which we have shown to be beneficial (Lutz et al. 2021). In the Australian Capital Territory, the Cotter catchment is a suitable recipient for migrants sourced from Cataract Dam, which harbours descendants of fish collected in the early 1900s from rivers in the region of the Cotter. In June 2017, 31 Macquarie perch were relocated from Cataract Dam and released into Cotter River in the ACT as part of the Genetic Rescue Research Project. Genetic management recommendations based on this project (Pavlova et al. 2017) are part of the national recovery plan for the species, and are being implemented in multiple jurisdictions. The project has produced a high-quality genome and detected a unique sex-determining mechanism in this species (Pavlova et al. 2021). Genomic data require massive computing infrastructure, as outlined in this ARDC publication.
Below is a graphic summary of some key points about this project. The people whose names are circled in red are key collaborators from management agencies with whom we co-design practical genetic rescue and its science.
Helmeted Honeyeater: Traditional conservation management has been successful in growing the last remaining population of HeHos. But we require a dramatic upturn of fortunes for sustainability into the future, and to reduce dependence on continuing management interventions. Genetic and field research indicates that managed gene flow from the most closely-related subspecies (L. m. gippslandicus) is unlikely to be harmful, and is the only population viability scenario that halts decline, with the potential to grow the population sufficiently to enable expansion to multiple sites. Comprehensive population monitoring of Helmeted Honeyeaters at Yellingbo presented a rare opportunity to estimate the negative effects of inbreeding over an individual's lifetime (Harrisson et al. 2019). We have demonstrated that the biology of HeHo impedes mate choices being good for genetic health of the population (Robledo-Ruiz et al. 2022a video abstract). The project has produced a high-quality genome, and extensive genome resources (Robledo-Ruiz et al. 2022b). Analyses are very advanced on the whole genomes of 75 HeHos and their relatives, funded by Helen Macpherson Smith Trust.
First release of 'genetically diverse' Helmeted Honeyeaters with mixed ancestry from two subspecies!
For a 3-minute summary of genetic rescue, with emphasis on Helmeted honeyeater, watch Diana Robledo Ruiz's very engaging video and 'My 3 favourite things about the helmeted honeyeater'.
Below is a graphic summary of some key points about this project. The people whose names are circled in red are key collaborators from management agencies with whom we co-design practical genetic rescue and its science.
Captive breeding trials conducted by our collaborators at Healesville Sanctuary, Zoos Victoria show that gene flow between subspecies improved fitness (Pavlova et al. 2023).
You can also read about this good news story hear.
Acknowledgements
This work would not be possible without the support of wildlife authorities including the Victorian Department of Environment, Land, Water and Planning, Parks Victoria, and the Australian Bird and Bat Banding Scheme. Monash ethics committees and ones from other institutions oversee ethical procedures and permissions. We thank collectors of all the specimens used from museums including the Museum of Victoria and the ethics and scientific research permit agencies that granted permits for those specimens to be collected.
This project is partially funded by ARC Linkage grant award LP160100482 2017-2020 and from the Partner Organizations DELWP, Zoos Victoria, DBCA, DArT P/L, ACT Government and University of Canberra.
PhD projects of Maiko Lutz, Joe Zilko, Diana Robledo Ruiz and Yael Rodger were supported by The Holsworth Wildlife Research Endowment & The Ecological Society of Australia.
Diana Robledo Ruiz and Yael Rodger received support grants for their projects from Parks Victoria. The Helen Macpherson Smith Trust Fund generously supported whole-genome resequencing to comprehensively address the question of what is genetically different about a Helmeted honeyeater compared to the rest of the species. This information will be used in forward genetic management of the birds.
Sasha Pavlova was generously supported by Revive & Restore.
Other funding has come from sources within Monash University, including support for student stipends and writing awards.
Many volunteers, collaborators and colleagues have contributed their time and other resources - many are co-authors on papers. The Friends of the Helmeted Honeyeater is an exceptionally effective community-based organization that working with agencies including DELWP, Zoos Victoria and Melbourne Water is creating landscape-scale improvements and habitat connection benefiting the ecological communities of which HeHos and Leadbeater's possums are part.
A previous partially-funded ARC Linkage grant LP110200017 ‘Genomics for persistence of Australian freshwater fish’ was important in creating background for this project, reflected in many of the key publications below.
Publications (many are open access, or otherwise available -see our PUBLICATIONS page for full details)
Frankham R, Ballou JD, Ralls K, Eldridge MDB, Dudash MR, Fenster CB, Lacy RC, Sunnucks P (2019) A Practical Guide for Genetic Management of Fragmented Animal and Plant Populations. Oxford University Press.
Frankham R, Ballou JD, Ralls K, Eldridge MDB, Dudash MR, Fenster CB, Lacy RC, Sunnucks P (2017) Genetic Management of Fragmented Animal and Plant Populations. Oxford University Press. INFORMATION
Garner BA, Hand BK, Amish SJ, Bernatchez L, Foster JT, Miller KM, Morin PA, Narum SR, O’Brien SJ, Roffler G, Templin WD, Sunnucks P, Strait J, Warheit KI, Seamons TR, Wenburg J, Olsen J, Luikart G (2016) Genomics in conservation: case studies for bridging the gap between data and application. Trends in Ecology and Evolution 31, 81-83.
Grueber CE, Sunnucks P. (2022). Using genomics to fight extinction. Science 376, 574-575.
Harrisson KA, Pavlova A, Telonis-Scott M, Sunnucks P (2014) Using genomics to characterize evolutionary potential for conservation of wild populations. Evolutionary Applications 7, 1008–1025
Harrisson KA, Pavlova A, Gonçalves da Silva A, Rose B, Bull JK, Lancaster ML, Murray ND, Quin B, Menkhorst P, Magrath M, Sunnucks P (2016) Scope for genetic rescue of an endangered subspecies though re-establishing natural gene flow with another subspecies. Molecular Ecology 25, 1242–1258
Harrisson KA, Pavlova A, Gan HM, Lee YP, Austin CM and Sunnucks P (2016) Pleistocene divergence across a mountain range and the influence of selection on mitogenome evolution in threatened Australian freshwater cod species. Heredity 116, 506 – 515.
Harrisson KA, Yen JDL, Pavlova A, Rourke ML, Gilligan D, Ingram BA, Lyon J, Tonkin Z, Sunnucks P (2016) Identifying environmental correlates of intra-specific genetic variation. Heredity 117, 155-164.
Harrisson KA, Magrath MJL, Yen JDL, Pavlova A, Murray N, Quin B, Menkhorst P, Miller KA, Cartwright K, Sunnucks P. (2019) Lifetime fitness costs of inbreeding and being inbred in a critically endangered bird. Current Biology 29, 1-7
Liddell E, Cook CN, Sunnucks P (2020). Evaluating the use of risk assessment frameworks in the identification of population units for biodiversity conservation. Wildlife Research 47: 208–216.
Liddell E, Sunnucks P, Cook CN (2021). To mix or not to mix gene pools for threatened species management? Few studies use genetic data to examine the risks of both actions, but failing to do so leads disproportionately to recommendations for separate management. Biological Conservation 256: 109072.
Lutz M, Tonkin Z, Yen JDL, Johnson G, Ingram B, Kearns J, Lyon J, Sunnucks P, Chapple DG, Pavlova A. (2021) Using multiple sources during reintroduction of a locally extinct population benefits survival and reproduction of an endangered freshwater fish. Evolutionary Applications 14, 950-964
Lutz ML, Sunnucks P, Chapple DG, Gilligan D, Lintermans M, Pavlova A, 2022. Strong bidirectional gene flow between fish lineages separated for over a 100,000 years. Conservation Genetics 23, 1105–1113
Mitchell WF, Boulton RL, Sunnucks P and Clarke RH. (2021) Are we adequately assessing the demographic impacts of harvesting for wild-sourced conservation translocations? Conservation Science and Practice, e569
Pavlova A, Sunnucks P (2022) Genetic rescue saves species from extinction. Scientia, March 2022.
Pavlova A, Selwood P, Harrisson KA, Murray N, Quin B, Menkhorst P, Smales I and Sunnucks P (2014) Integrating phylogeography and morphometrics to assess conservation merits and inform conservation strategies for an endangered subspecies of a common species. Biological Conservation 174, 136–146.
Slide and audio summary small filesize large filesize
Pavlova A, Beheregaray LB, Coleman R, Gilligan D, Harrisson KA, Ingram BA, Kearns J, Lamb AM, Lintermans M, Lyon JP, Nguyen TTT, Sasaki M, Tonkin Z, Yen JDL and Sunnucks P (2017) Severe consequences of habitat fragmentation on genetic diversity of an endangered Australian freshwater fish: a call for assisted gene flow. Evolutionary Applications, 10, 531–550
Pavlova A, Gan HM, Lee YP, Austin CM, Gilligan D, Lintermans M, Sunnucks P (2017) Purifying selection and drift shaped Pleistocene evolution of mitochondrial genome in an endangered Australian freshwater fish. Heredity 118, 466-476
Pavlova A, Harrisson KA, Turakulov RI, Lee YP, Ingram BA, Gilligan D, Sunnucks P, Gan MH (2022) Labile sex chromosomes and a novel candidate sex-determination gene in the Australian freshwater fish family Percichthyidae. Molecular Ecology Resources, 22, 1639-1655. MER-21-0339
Pavlova A, Petrovic S, Harrisson KA, Cartwright K, Dobson E, Hurley LL, Lane M, Magrath MJL, Miller KA, Quin B, Winterhoff M, Yen JDL, Sunnucks P (2023). Benefits of genetic rescue of a critically endangered subspecies from another subspecies outweigh risks: Results of captive breeding trials. Biological Conservation https://doi.org/10.1016/j.biocon.2023.110203
Pierson JC, Beissinger SR, Bragg JG, Coates DJ, Oostermeijer JGB, Sunnucks P, Schumaker NH, Trotter MV, Young AG (2015) Incorporating evolutionary processes into population viability models: Eco-Evo PVAs. Conservation Biology 29, 755–764.
Pierson JC, Coates DJ, Oostermeijer JGB, Beissinger SR, Bragg JG, Sunnucks P, Schumaker NH, Young AG (2016) Consideration of genetic factors in Threatened Species Recovery Plans on three continents. Frontiers in Ecology and the Environment 14: 433–440
Radford JQ, Amos JN, Harrisson KA, Sunnucks P and Pavlova A (2021) Functional connectivity and population persistence in woodland birds: Insights for management from a multi-species conservation genetics study. Emu – Austral Ornithology, 121, 147-159.
Ralls K, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC, Sunnucks P, and Frankham R. (2018) Call for a paradigm shift in the genetic management of fragmented populations. Conservation Letters 11, 1-6.
Ralls K, Sunnucks P, Lacy RC, Frankham R (2020). Genetic rescue: A critique of the evidence supports maximizing genetic diversity rather than minimizing the introduction of putatively harmful genetic variation. Biological Conservation 251: 108784.
Robledo‐Ruiz DA, Pavlova A, Clarke RH, Magrath MJl, Quin B, Harrisson KA, Gan HM, Low GW, Sunnucks P. (2022a) A novel framework for evaluating in‐situ breeding management strategies in endangered populations. Molecular Ecology Resources, 22, 239-253. near-final version see video abstract
Robledo-Ruiz DA, Gan HM, Kaur P, Dudchenko O, Weisz D, Khan R, Lieberman-Aiden, Osipova E, Hiller M, Morales HE, Magrath MJL, Clarke RH, Sunnucks P, Pavlova A. (2022b) Chromosome-length genome assembly and linkage map of a Critically Endangered Australian bird: the helmeted honeyeater. GigaScience 11.
explainer video GigaScience blog Press release
Robledo-Ruiz DA, Austin L, Amos JN, Castrejón-Figueroa J, Harley DKP, Magrath MJL, Sunnucks P, Pavlova A, 2023. Easy-to-use R functions to separate reduced-representation genomic datasets into sex-linked and autosomal loci, and conduct sex-assignment. Molecular Ecology Resources published online 2/08/2023. http://doi.org/10.1111/1755-0998.13844.
Rodger YS, Pavlova A, Sinclair S, Pickup M, Sunnucks P. (2021) Evolutionary history and genetic connectivity across highly fragmented populations of an endangered daisy. Heredity, 126, 846–858. Data. Nature Blog
Roitman M, Gardner MG, New TR, Nguyen TTT, Roycroft EJ, Sunnucks P, Yen AL, Harrisson KA. (2017) Assessing the scope for genetic rescue of an endangered butterfly: the case of the Eltham copper. Insect Conservation and Diversity 10, 399–414
Yen JDL, Todd CR, Sharley J, Harris A, Geary WL, Kelly E, Pavlova A, Hunt TL, Ingram B, Lyon, J, Tonkin Z (2022). Establishing new populations in water-secure locations may benefit species persistence more than interventions in water-stressed locations. Biological Conservation 276, 109812.
Zander KK, Peterson St-Laurent G, Hogg CJ, Sunnucks P, Woinarski JCZ, Legge S, Burton M, Pandit R, Hagerman S, Garnett ST (2021) Measuring social preferences for conservation management in Australia. Biological Conservation, 262, 109323.
Zilko JP, Harley D, Hansen B, Pavlova A, Sunnucks P. (2020) Accounting for cryptic population structure enhances detection of inbreeding depression with genomic inbreeding coefficients: an example from a critically endangered marsupial. Molecular Ecology 29, 2978–2993
Zilko JP, Harley D, Pavlova A, Sunnucks P. (2021) Applying population viability analysis to inform genetic rescue that preserves locally unique genetic variation in a critically endangered mammal. Diversity 13, 382.