The semi-aquatic platypus (Ornithorhynchus anatinus), along with echidnas, belong to the order Monotremata, the most species-scarce (n = 5) and most basal branch of the mammalian group, which diverged from marsupials and eutherians 187 Mya (Zhou et al., 2021). Platypuses have a unique combination of features, including oviparity, venomous spurs in males, electroreception used to locate freshwater macroinvertebrates, biofluorescent pelage, and multiple sex chromosomes (five pairs instead of one; Veyrunes et al., 2008; Bino et al., 2019; Anich et al., 2021). The uniqueness and rarity of platypus features (sensu Pavoine et al., 2005) and the longest evolutionary history in mammals (97.6 million years; Isaac et al., 2007) make it arguably the most irreplaceable mammal existing today.
There is increasing evidence of larger numbers of platypuses in historical times and ongoing declines and extinctions of local populations (Grant & Fanning, 2007; Bino et al., 2019; Hawke et al., 2019; Bino et al., 2020). Declines are likely driven by multiple and synergistic threats, including river regulation, habitat modification, climate change, pollution, by-catch mortality, and predation by invasive species (Grant & Fanning, 2007; Bino et al., 2019; Hawke et al., 2019; Bino et al., 2020). Continued declines due to current and future climate change are predicted as a result of increased frequency and severity of droughts (Bino et al., 2019; Bino et al., 2021; Hawke, Bino, & Kingsford, 2021a), as well as elevated temperature conditions which could lead to the loss of more than 30% of suitable habitat by 2070 (Klamt et al., 2011; Hawke, Bino, & Kingsford, 2021a).
The platypus is currently listed as ‘Near Threatened’ by the International Union for Conservation of Nature (IUCN; Woinarski & Burbidge, 2016), ‘Endangered’ in South Australia (National Parks and Wildlife Act 1972), ‘Vulnerable’ in Victoria (Victoria Government Gazette, 2021). Past threats include hunting for fur, while present threats include extensive habitat degradation by agriculture and urbanisation, regulation of water flows, by-catch mortality in fishing gear, diseases, and predation by invasive foxes and dogs (Grant & Temple-Smith, 2003; Bino et al., 2019; Hawke, Bino, & Kingsford, 2021a).
Moreover, all these threats have possibly been intensified by the construction of major dams that have immediate and long-term effects, being one of the more serious threats for platypus conservation, given their likely broad impact on habitat (Grant & Temple-Smith, 2003; Bino et al., 2019; Hawke, Bino, & Kingsford, 2021a). Major dams are widespread across much of the platypus distribution, where as many as 77% (383 out of 495) of the Australian major dams (wall height > 10 m; ancold.org.au) coincide within the regions where platypuses occur (Fig. 1a; see also Bino et al., 2020). Immediate adverse effects of major dams extend over large areas both upstream and downstream. Water impoundments behind major dams form wind-exposed, deep, and standing (lentic) ecosystems. Below major dams, altered natural flow regimes can significantly impact platypus abundances and demographics (Hawke, Bino, & Kingsford, 2021b). Conditions below and above major dams represent poor foraging and burrowing habitat for platypuses, given lower productivity of macroinvertebrate prey species (Grant & Llewellyn, 1991; Bethge et al., 2003; Grant, 2004; Grant & Fanning, 2007; Marchant & Grant, 2015).
Long-term effects of major dams include reduction in the ability of platypuses to move between potential habitat areas. This fragmentation has twofold effects; first, it restricts the ability to recolonise available habitat or migrate to areas with more suitable conditions (Baguette et al., 2013). Secondly, and importantly, fragmentation also simultaneously reduces both local population size and gene flow, each of which is expected to lead to increased inbreeding and reduction of the genetic variation necessary for adaptation to changes including threats (Frankham et al., 2017). One adverse consequence of small population size is lower survival and lower reproduction output due either to inbreeding depression or to catastrophic stochastic events. Another adverse consequence is reduced variation between individuals, necessary for adaptation to changes such as the threats listed above (Frankham, 2015). These genetic changes may be prevented by immigration because gene flow replenishes the gene pool of populations, but of course, this will only happen if the small population is not a fragmented isolate (Garant et al., 2007; Tigano & Friesen, 2016).
For platypuses, major dams are predicted to be a barrier for dispersal (Kolomyjec, 2010; Furlan et al., 2013), with potential long-term ramifications for gene flow, genetic variation, and adaptation to threats as described above. However, both the restriction of dispersal and the genetic consequences remain largely unquantified. Population viability analyses suggest significant impacts by major dams, particularly in synergy with lower habitat quality and droughts, which are projected to increase (Bino et al., 2020). However, the extent to which major dams restrict platypus dispersal remains unclear because landscape connectivity varies due to both the species’ life history and landscape features (Baguette et al., 2013). Platypuses are known to climb around dams up to 10m high (Jenolan Karst Conservation Reserve Newsletter, https://sway.office.com/qI6BOrvW8CO5vS8i?ref=email), although their ability to find their way around higher structures is currently unknown. Their ability to swim across the large deep-water impoundments above the dam is unclear.
Therefore, our research uses genetic methods to focus on the connectivity of platypus populations above and below major dams. Genetic-based methods used to infer patterns of dispersal and gene flow (Balkenhol et al., 2015) commonly examine the positive relationship between the amount of genetic differentiation between populations or individuals and the geographic distance separating them (Ramachandran et al., 2005). The presence of a dispersal barrier could be inferred by testing whether populations or individuals, separated by potential barriers, are more genetically differentiated than populations or individuals in landscapes lacking such barriers but separated by a similar distance. Genetic differentiation can increase due to dispersal barriers within one to 15 generations during simulations (Landguth et al., 2010), but is unlikely to arise if population size is large (> 50 individuals) or if the species lifespan is long (> 22 years; Hoffman et al., 2017).
To determine whether major dams have reduced dispersal and gene flow between platypus groups, we analysed genetic data from platypuses sampled in nine rivers; five rivers were regulated by major dams, and four were unregulated (Fig. 1). If major dams adversely affected gene flow between platypus groups, we predicted the following: a) individuals and groups separated by a major dam in a river should be more differentiated than in an unregulated river, and; b) genetic differentiation across major dams should correlate with the time since the dam was built.