Population Genetics of a Widely Distributed Small Freshwater Fish with Varying Conservation Concerns: the Southern Purple- Spotted Gudgeon, Mogurnda Adspersa

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Population Genetics of a Widely Distributed Small Freshwater Fish with Varying Conservation Concerns: the Southern Purple- Spotted Gudgeon, Mogurnda Adspersa Population genetics of a widely distributed small freshwater fish with varying conservation concerns: the southern purple- spotted gudgeon, Mogurnda adspersa Minami Sasaki, Michael P. Hammer, Peter J. Unmack, Mark Adams & Luciano B. Beheregaray Conservation Genetics ISSN 1566-0621 Conserv Genet DOI 10.1007/s10592-016-0829-2 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Conserv Genet DOI 10.1007/s10592-016-0829-2 RESEARCH ARTICLE Population genetics of a widely distributed small freshwater fish with varying conservation concerns: the southern purple-spotted gudgeon, Mogurnda adspersa 1 2 3 4,5 Minami Sasaki • Michael P. Hammer • Peter J. Unmack • Mark Adams • Luciano B. Beheregaray1 Received: 28 October 2015 / Accepted: 25 February 2016 Ó Springer Science+Business Media Dordrecht 2016 Abstract Genetic variation plays a pivotal role in species individuals; 35 localities). The results consistently indi- viability and the maintenance of population genetic varia- cated very low levels of genetic variation throughout, tion is a main focus of conservation biology. Threatened including along the east coast where the species is rela- species often show reduced genetic variation compared to tively common. At the broader scale, three highly differ- non-threatened species, and this is considered indicative of entiated groups of populations were found, concordant with lowered evolutionary potential, compromised reproductive previously reported genealogical distinctiveness. Hence we fitness, and elevated extinction risk. The southern purple- propose each group as a distinct Evolutionarily Significant spotted gudgeon, Mogurnda adspersa, is a small freshwater Unit. We also inferred a minimum of 12 management units fish with poor dispersal potential that was once common in M. adspersa, with no appreciable gene flow between throughout the Murray–Darling Basin (MDB) and along them. Our study discloses findings relevant for both long- the central east coast of Australia. Its numbers and distri- and short-term management, as it informs on the geo- bution have shrunk dramatically in the MDB due to flow graphic context in which conservation priorities should be alteration, degradation of habitat, decreasing water quality, defined and specifies biological units for population mon- and introduction of alien species. We used microsatellite itoring and translocations. DNA markers to assess population structure and genetic variation at both large (i.e. across basin) and fine (i.e. Keywords Conservation genetics Á Freshwater fish Á within river catchments) spatial scales using a substantial Endangered biodiversity Á Ecological genetics Á sampling effort across the species range (n = 579 Phylogeography Á Population connectivity Electronic supplementary material The online version of this Introduction article (doi:10.1007/s10592-016-0829-2) contains supplementary material, which is available to authorized users. Genetic diversity is known to play a pivotal role in species & Luciano B. Beheregaray viability, and thus the maintenance of genetic variability at Luciano.Beheregaray@flinders.edu.au the population level is a key focus of conservation biology 1 Molecular Ecology Laboratory, School of Biological (Avise 2004; Frankham et al. 2002). Genetic diversity Sciences, Flinders University, Adelaide, SA 5001, Australia reflects variability in heritable characters, including phe- 2 Curator of Fishes, Museum and Art Gallery of the Northern notypes and DNA sequence variation (Frankham et al. Territory, Darwin, NT 0801, Australia 2002). Many factors and processes influence spatial and 3 Institute for Applied Ecology, University of Canberra, temporal variations in levels of genetic diversity. In par- Canberra, ACT 2601, Australia ticular, gene flow and genetic drift are two of the main 4 Australian Centre for Evolutionary Biology and Biodiversity, microevolutionary processes affecting levels of genetic University of Adelaide, Adelaide, SA 5005, Australia diversity between and within populations (Hedrick 2009). 5 Evolutionary Biology Unit, South Australian Museum, Gene flow strongly influences pattern and process of Adelaide, SA 5000, Australia population genetic structure and can in principle be 123 Author's personal copy Conserv Genet quantified by assessing levels of genetic differentiation while drought exacerbates this loss of connectivity and between populations. Gene flow can introduce new alleles habitat loss for many freshwater species (Cai and Cowan to genetically different populations, and hence increase 2008). genetic diversity (Frankham et al. 2002). Gene flow also Reflecting a continent with comparatively low rainfall shapes metapopulation dynamics in which local extinction and a high proportion of its population and agriculture can be rescued by recolonization (Hanski 1998). Obvi- concentrated in the drier southern half, Australia’s tem- ously, rates of gene flow vary among species and are perate freshwater systems have been heavily impacted by critically dependant on life history, local environment and all of the above-mentioned causes of habitat fragmentation. biogeography. Most Australian temperate catchments have experienced For isolated populations, genetic drift is perhaps the extensive river modifications (Lloyd et al. 2004), and crucial factor shaping levels of genetic diversity and evo- recent extreme droughts have cumulated in critical lutionary potential (Hedrick 2009). A completely isolated impacts, especially in the heavily modified Murray–Dar- population i.e. where there is no gene flow between pop- ling Basin (MDB) (e.g. Hammer et al. 2013; Ellis et al. ulations, is the most severe form of fragmentation 2013; Kingsford et al. 2011). To explore the consequences (Frankham et al. 2002). Populations in such a fragmented of fragmentation on the aquatic fauna of this region, we state may suffer strongly from a loss of genetic diversity investigated population connectivity and genetic diversity due to the stochastic effects of genetic drift, whereas in a small Australian freshwater fish, the southern purple increased allelic similarity due to inbreeding may lead to spotted-gudgeon, Mogurnda adspersa, as a model species population extinctions (Frankham et al. 2002). The rate of to link broad- and fine-scale patterns of population isola- such effects is faster in smaller populations because the tion to species and habitat conservation. likelihood of allele loss is higher when effective population Mogurnda adspersa is a habitat specialist that requires sizes (Ne) are small (Hughes et al. 1999; Frankham et al. dense cover in the form of physical elements and aquatic 2002; Hedrick 2009). The resultant inbreeding may lead to vegetation in off-channel wetland habitats (Hammer et al. reductions in fecundity, survival of young, and body size 2015). The species displays an idiosyncratic distribution (Amos and Balmford 2001; Weiss 2005; Thrower and Hard pattern of being a widespread species with very limited 2009) due to deleterious allele combinations. Small popu- dispersal ability (Hughes et al. 2012; Shipham et al. 2013). lations under the influence of the above effects are also The species as currently defined (Allen and Jenkins 1999) susceptible to disease and stochastic events (Frankham occurs in tropical to temperate coastal drainages in Eastern 2003) and, as a consequence, the number of reproductive Australia, and into the inland MDB. However, there is individuals (Ne) decreases even more. Importantly, the genetic evidence of a species level divide north and south residual consequences due to reduction in Ne will persist of the Burdekin Gap on the east coast (Adams et al. 2013), for a long time, even if the original cause of population and additional strong phylogeographic signal within the fluctuation is eliminated (Frankham 2003). southern candidate taxon suggesting that populations in the Understanding the potential genetic effects of isolation MDB were separated from coastal populations approxi- is important for the conservation and management of spe- mately 1.4–1.8 million years ago (Faulks et al. 2008). cies, and is a particular challenge for freshwater organisms There are contrasting conservation concerns between these due to the highly structured and variable nature of the coastal and inland lineages, with M. adspersa considered environment. Unlike terrestrial or marine environments, common on the east coast (apart from possible local rivers form a dendritic network in which the movement of extinction in the Richmond and Clarence rivers, New South species is restricted (Fagan 2002; Hughes et al. 2009). Wales: Pusey et al. 2004), but endangered in the MDB Correspondingly, freshwater species such as fishes often following a dramatic decline in numbers and distribution display low intra-population and high inter-population being
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