Surprising Pseudogobius: Molecular systematics of benthic gobies reveals new insights into estuarine biodiversity (Teleostei: Gobiiformes)

https://doi.org/10.1016/j.ympev.2021.107140Get rights and content

Highlights

  • Extensive sampling of estuarine gobies around the Australian coastline.

  • Multiple lines of evidence for at least six cryptic species.

  • Major unrealized biodiversity occurs in the region and potentially abroad.

  • Diverse estuarine faunas need consideration with future development and management.

Abstract

Snubnose gobies (genus Pseudogobius: Gobionellinae) are ubiquitous to, and important components of, estuarine ecosystems of the Indo-west Pacific. These small benthic fishes occur in freshwater, brackish and marine habitats such as mangroves, sheltered tide pools and lowland streams, and represent a model group for understanding the biodiversity and biogeography of estuarine fauna. To develop the species-level framework required for a concurrent morphological taxonomic appraisal, we undertook thorough sampling around the extensive Australian coastline, referenced to international locations, as part of a molecular systematic review using both nuclear and mitochondrial markers. The results indicate that while there are currently eight recognised species, the true diversity is close to double this, with a hotspot of endemism located in Australia. Complicated patterns were observed in southern Australia owing to two differing zones of introgression/admixture. Key drivers of diversity in the group appear to include plate tectonics, latitude, and historic barriers under glacial maxima, where an interplay between ready dispersal and habitat specialisation has led to regional panmixia but frequent geographic compartmentalisation within past and present landscapes. The findings have significant implications for biodiversity conservation, coastal and estuarine development, the basic foundations of field ecology, and for applied use such as in biomonitoring.

Introduction

Marine and freshwater fishes are known to differ widely in their levels of dispersal-driven genetic structure, with marine species typically displaying more homogenous patterns compared to the often pronounced substructure displayed by freshwater taxa (Ward et al., 1994). However, predicting the spatial genetic patterns of estuarine fishes straddling these two environments is more challenging, owing to potential conflicts between traits helpful for marine dispersal (e.g. small pelagic larvae, adult mobility), and factors that tend to enhance genetic isolation such as habitat specificity (e.g. water quality, sheltered environments, vegetation), currents, distance and biogeographic barriers (Watts and Johnson, 2004). Further, ecological understanding of estuarine species, including species richness and conservation needs, can be limited due to the sometimes difficult-to-sample nature of these habitats, especially in the tropics (e.g. thick anoxic mud, turbid water, biting insects, crocodiles) (Blaber, 2002). Molecular systematics can thus offer important evolutionary insights into estuarine biodiversity pattern and process, including gene flow and the presence of cryptic species (Beheregaray and Sunnucks, 2001, Bilton et al., 2002).

One group of small benthic fishes, the gobionelline gobies (Gobiidae), is prominent in estuarine environments of the Indo-west Pacific, being ubiquitous to habitats such as sheltered rock pools, tidal estuaries, mangroves, coastal lagoons, and the lower portions of streams. Some 370 species in 55 genera are estimated to occur (Pezold, 2011), with species discovery ongoing (e.g. Larson, 2001, Larson, 2009, Larson, 2010). Awaiting revision are the snubnose gobies of the genus Pseudogobius Popta 1922, being a particularly wide-spread and common representative of the sub-family distributed from Japan to southern Australia and Pakistan across to Vanuatu (Fig. 1). Members of the genus (typically 2–6 cm in total length) appear to share general biological traits of demersal adhesive eggs, small (<2 mm) pelagic larvae, benthic adults and vegetarian/omnivorous diets (Neira and Potter, 1992, Gill and Potter, 1993, Gill et al., 1996, Close and Gouws, 2007). Specialisation for estuarine conditions (Potter et al., 2015) such as for shelter, moderate salinity, or habitat types (e.g. aquatic macrophytes, mangroves) has been suggested (Gill and Potter, 1993, Yokoo et al., 2008).

As with many small gobies, there has been some historical confusion in the taxonomic placement, description, and identification of Pseudogobius species. Larson (2001) provisionally identified six valid species (Pseudogobius avicennia (Herre 1940), Pseudogobius javanicus (Bleeker 1856), Pseudogobius olorum (Sauvage 1880), Pseudogobius masago (Tomiyama 1936), Pseudogobius melanosticta (Day 1876) and Pseudogobius poicilosoma (Bleeker 1849)), and there have been two recent descriptions (Pseudogobius fulvicaudus Huang, Shao & Chen 2014 and Pseudogobius taijiangensis Chen, Huang & Huang 2014), in part diagnosed with molecular data (Chen et al., 2014, Huang et al., 2014).

The expansive Australian coastline, covering almost 60,000 km when its islands are included, offers a unique study setting for better understanding patterns of biodiversity in estuarine fishes (Gill and Potter, 1993, Pusey et al., 2015). The region spans a range of climatic and biogeographic zones, from monsoon tropics to cool temperate, and variable levels of human-induced landscape change; more intensive in the south-east. The most obvious biogeographic feature in Australia is the north-south faunal division relating to climate (Tropic of Capricorn, 23°5′ S), with a range of major biogeographic provinces and features recorded for marine and freshwater species respectively (Wilson and Allen, 1987, O'Hara and Poore, 2000, Unmack, 2001, Commonwealth of Australia, 2005, Poore and O’Hara, 2007, Waters et al., 2010b). Presently only two species of Pseudogobius are listed for Australia, the southern endemic P. olorum and P. poicilosoma from northern Australia, New Guinea and Java (Larson, 2001). However, at least two additional undescribed species have been touted, a bluespot goby Pseudogobius ‘sp. 9’ from southeastern Australia (Larson and Hoese, 1996) and a dwarf mangrove dwelling species Pseudogobius ‘sp. 3’ from the Northern Territory (Larson et al., 2013).

The current study examines genetic diversity in Pseudogobius to provide a systematic framework for ecology and conservation management. Our objectives are to assess species boundaries to guide concurrent morphology-based taxonomic revision (Larson and Hammer, in prep.), explore evolutionary relationships in the genus, and examine the influence of major biogeographic features. Through targeted sampling around almost the entire Australian coastline (Fig. 1, Fig. 2), we specifically predict that due to coastal occurrence and pelagic larvae the signature of regional isolation (i.e. cryptic allopatric species and major sub-structure) will be less evident in Pseudogobius compared to co-occurring freshwater restricted species (Adams et al., 2013, Shelley et al., 2018, Hammer et al., 2019), but that the traits of small size, benthic nature, and potential estuarine specialisation will counter any expectation that wide-spread species display panmixia (e.g. McGlashan and Hughes, 2001, Roberts and Ayre, 2010). Multiple nuclear markers were selected to evaluate contemporary gene flow and diagnose species boundaries in Australia (Waters et al., 2010a, Wallis et al., 2017), contrasted and supplemented with mitochondrial DNA data for a broader evolutionary and geographic context (Cook et al., 2010, Adams et al., 2014, Hammer et al., 2019).

Section snippets

Field sampling

Field sampling utilised seine and dip nets covering a range of estuarine habitat types, typically accessed from shore, and sampled at low tide when fish are concentrated or in isolated habitats, thus making sampling either more effective or possible (e.g. to avoid Saltwater Crocodiles Crocodylus porosus in the tropics). Where possible for relatively larger fish, a paired tissue/voucher system was used – each individual had a small fillet removed from the right-hand side of the body, with

Nuclear data

The final allozyme dataset for the northern overview study comprised 51 fish genotyped for 55 putative loci (summary of allozyme frequencies by taxon in Table S1). The four southern exemplars also included in this study were substantially divergent from all northern fish (fixed differences at ~60–70% of loci examined). One Australian OTU, Pseudogobius sp. 3, could not be verified with nuclear data due to a lack of frozen tissues. An initial PCoA for the northern overview study (Fig. S1)

Discussion

Genetic data from both nuclear and matrilineal markers demonstrate that current knowledge severely underestimates the number of species of the estuarine goby genus Pseudogobius. The observed spatial patterns of genetic division and sub-structure shed light on inadequacies with the taxonomic framework for the group, the conservation and management of estuarine species and habitats, and the relative influence of dispersal, habitat, and connectivity in estuarine conditions, particularly for

CRediT authorship contribution statement

Michael P. Hammer: Conceptualization, Investigation, Resources, Data curation, Visualization, Writing - original draft, Writing - review & editing, Funding acquisition, Project administration. Mark Adams: Conceptualization, Formal analysis, Investigation, Resources, Visualization, Writing - original draft, Writing - review & editing. Peter J. Unmack: Investigation, Resources, Writing - review & editing. Kathryn L. Hassell: Investigation, Resources, Writing - review & editing. Terry Bertozzi:

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We acknowledge Traditional Owners and land managers of our study region and recognise their continuing connection to land and water. Helen Larson provided valuable input on taxonomy and field identification. The collation of samples involved the contribution of many people. International samples were supplied by Koichi Shibukawa, Josh Egan, Andrew Storey and Gianluca Polger and sourced on collection trips by Helen Larson, including the Singapore Biodiversity Workshop, and by PJU in Papua New

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