Evaluating the genetic consequences of population subdivision as it unfolds and how to best mitigate them: a rare story about koalas.
Frère, C.H.1; O’Reilly, G.D. 2; Strickland, K. 3; Schultz, A.4; Hohwieler, K5.; Hanger, J. 6; de Villiers, D. 6; Cristescu, R. 5; Powell, D.5 and Sherwin, W. 2
  1. School of Biological Sciences, University of Queensland, St Lucia, QLD, Australia.
  2. The School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, Australia.
  3. Institute of Ecology and Evolution, University of Edinburgh, Edinburgh, UK
  4. Icelandic Museum of Natural History (Náttúruminjasafn Íslands), Reykjavik, Iceland
  5. School of Science, Technology and Engineering, University of the Sunshine Coast, Queensland, Australia.
  6. Endeavour Veterinary Ecology Pty Ltd, Toorbul, QLD, Australia
Corresponding author: c.frere@uq.edu.au
Authors contribution:
CHF: study design, analyses, SNP genotyping, manuscript write up and editing
GOD: study design, analyses, manuscript write up and editing
KS: study design, analyses, manuscript write up and editing
AS: SNP genotyping, analyses, manuscript editing
KH: analyses, manuscript editing
JH: sample collection, manuscript editing
DD: analyses, sample collection, manuscript editing
RC: manuscript editing
DP: analyses, SNP genotyping and manuscript editing
WS: study design, analyses, manuscript editing
Abstract.
The genetic consequences of the subdivision of populations are regarded as significant to long-term evolution, and research has shown that the scale and speed at which this is now occurring is critically reducing the adaptive potential of most species which inhabit human impacted landscapes. Here, we provide a rare, and to our knowledge, the first analysis of this process while it is happening and demonstrate a method of evaluating the effect of mitigation measures such as fauna crossings. We did this by using an extensive genetic dataset collected from a koala population which was intensely monitored during the construction of linear transport infrastructure which resulted in the subdivision of their population. First, we found that both allelic richness and effective population size decreased through the process of population subdivision. Second, we predicted the extent to which genetic drift could impact genetic diversity over time and showed that after only 10 generations the resulting two subdivided populations could experience between 12-69% loss in genetic diversity. Lastly, using forward simulations we estimated that a minimum of 8 koalas would need to disperse from each side of the subdivision per generation to maintain genetic connectivity close to zero but that 16 koalas would ensure that both genetic connectivity and diversity remained unchanged. These results have important consequences for the genetic management of species in human impacted landscapes by showing how to assess the immediate and longer-term genetic consequences of population subdivision as it is occurring, and how to evaluate the effectiveness of any mitigation measures.
Introduction.
Subdivision of wild populations, and its genetic consequences, are regarded as significant for long-term evolution (Orr & Coyne 2004) and shorter-term conservation because the scale and speed at which this is now occurring is critically reducing the adaptive potential of most species which inhabit human impacted landscapes (Frankham et al.2017; Johnson & Munshi-South 2017; Miles et al. 2019; Schellet al. 2021). The construction of linear transport infrastructure (e.g. road, railways), for instance, stands as one of the main culprits of anthropogenically caused biodiversity decline (Haddad et al.2015; Torres et al. 2016). Because it fragments landscapes, linear transport infrastructure ultimately results in a myriad of direct and indirect ecological consequences for wildlife, including, but not limited to, increased mortality and injury through road kill (Glistaet al. 2009; Beebee 2013; Loss et al. 2014; Pinto et al. 2018), decreased dispersal abilities (Chen & Koprowski 2016) and an increase in the impact of genetic drift, reduced genetic diversity and limited gene flow (Dixo et al. 2009; Miles et al.2019; Schmidt et al. 2020). As transportation networks continue to grow so will biodiversity decline (Haddad et al. 2015; Torreset al. 2016; Pimm et al. 2021), making the need to understand and mitigate their impact on species an urgent focus for conservation worldwide (Haddad et al. 2015; Wilson et al.2016; Brady & Richardson 2017; Barrientos et al. 2021). We provide here a rare analysis of the genetic consequences of population subdivision by linear transport infrastructure while it is happening and demonstrate a method of evaluating the effect of mitigating measures such as purpose-built fauna crossing structures.
There are now many types of purpose-built fauna crossing structures used across the world, such as underpasses and overpasses (Pimm et al.2021), with one common goal, facilitating animal movement across linear transport infrastructure with the aim to restore habitat connectivity across road networks. While research has shown that animals use these purpose-built structures (Lesbarrères & Fahrig 2012; Pimm et al.2021), we have also learned that their use is heavily influenced by their design (Cain et al. 2003; Clevenger & Waltho 2005), their placement (Rodriguez et al. 1996; Clevenger & Waltho 2000) and the biology of the target species (Dexter et al. 2016). Our understanding of their effectiveness in preventing the longer-term impacts of linear transport infrastructure on habitat connectivity via gene flow, however, remains poorly understood (Soanes et al.2018; Pimm et al. 2021). This is because we cannot assume that restoring animal movement across linear transport infrastructure will necessarily translate into gene flow. Indeed, Riley et al. (Rileyet al. 2006) showed how despite moderate levels of migration across one of the busiest highways in America, populations of carnivores on either side remained genetically differentiated, because migrating individuals rarely reproduced.
We know that maintaining genetic connectivity in human-impacted landscape is key to wildlife conservation (Brady & Richardson 2017; Johnson & Munshi-South 2017; Miles et al. 2019; Fusco et al. 2021). By creating a patchwork of small isolated populations with reduced exchange (Riley et al. 2006; Miles et al. 2019; Fusco et al. 2021), linear transport infrastructure networks have now been shown to cause a range of genetic consequences for species including increased inbreeding (Larison et al. 2021; Connoret al. 2022), increased genetic drift (Miles et al. 2019) and decreased effective population size (Ne) (Trumboet al. 2019), all of which can have deleterious consequences on species (Margan et al. 1998). While these studies have provided a significant step toward understanding the genetic consequences of human-induced habitat fragmentation on wildlife retrospectively, its study would benefit from understanding its effect on patterns of genetic diversity while population subdivision is taking place. This is because changes and their ecological and genetic consequences are often discovered after the subdivision has already occurred and not whilst it is occurring. Here, we use a rare genetic dataset collected on a large population of free-ranging koalas (Phascolarctos cinereus ) which documents the process of population subdivision as it occurred (before, during and after division) to ask three specific questions about the genetic consequences of population subdivision by linear transport infrastructure and how it could be mitigated:
  1. What are the immediate genetic consequences of the population subdivision?
  2. What are the longer-term genetic consequences of the population subdivision?
  3. What extent of dispersal would be required to maintain/restore genetic connectivity and diversity between the now subdivided populations located on either side of (‘above’ and ‘below’) the linear transport infrastructure?
We were able to ask these questions because of the rareness of the dataset which was obtained during and after construction of a linear transport infrastructure (e.i. rail line) which resulted in the subdivision of a large population of koala. The dataset was collected as part of an extensive Koala Management Program (Beyer et al.2018), in which all free-ranging koalas (Phascolarctos cinereus ; n = 503 koalas) were captured and healthy animals released and monitored between 2013 and 2017 for the purpose of a rail infrastructure project located in Queensland, Australia. These koalas formed part of a single breeding population (Schultz et al. 2022) inhabiting a mixture of urban and peri-urban koala habitat remnants along 12.6 kms of the linear transport infrastructure project footprint (Hanger et al. 2017). Koala-proof fencing was installed alongside the rail line corridor to prevent koala death from crossing attempts, and underpasses were built at strategic locations along the rail line (Hanger et al. 2017). Because all koalas were VHF and/or GPS tracked during all phases of construction (pre, during and post), it afforded us detailed knowledge of how and why the impacted koala population’s size varied throughout the rail line construction phases: (1) all deaths and births and causes of death (Hanger et al. 2017; Beyer et al.2018), (2) which koalas were translocated as a result of the rail line infrastructure project, (3) their locations pre and post-construction (whether koalas occupied habitat on one side or the other of the rail line), and (4) rail crossing events by koalas after establishment of the rail barrier using both dedicated fauna crossings and hydrology culverts (Dexter et al. 2017). In total, 291 koalas out of the 503 processed (57.8% population size decline) died or were euthanised during the four-year monitoring program: 182 from predation, 84 from disease, 14 from trauma, and 11 unknown causes of death (Beyer et al. 2018). Twenty-eight were translocated as a result of their core home range directly overlapping with the rail line and/or because current land-use and imminent future land-use precluded their long-term viability if left in situ . This left 102 koalas that were previously genetically connected, then became subdivided on either side of the rail-line.
Method