Environment Institute Leaders publications

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A molecular systematic overview of wolf spiders associated with Great Artesian Basin springs in South Australia: evolutionary affinities and an assessment of metapopulation structure in two species
(C S I R O Publishing, 2008) Gotch, T.; Adams, M.; Murphy, N.; Austin, A.
The molecular genetic techniques of allozyme electrophoresis and mitochondrial DNA sequencing were used to examine species boundaries, phylogenetic affinities, and population structure in wolf spiders associated with artesian springs of the Great Artesian Basin (GAB) in South Australia. These springs contain the only permanent water in this extremely arid region, and consequently are of great biological, economic, and sociological significance. Molecular diagnoses of species boundaries in nine lycosid species, involving 56 individuals genotyped at 37 putative allozyme loci and 21 individuals sequenced for a ~600-bp portion of nicotinamide adenine dinucleotide dehydrogenase 1 (NADH1), were largely concordant with those recently proposed on morphological criteria. They also identified a species not previously collected, and suggested that GAB and mesic forms of Venatrix arenaris (Hogg) may not be conspecific. As well as insights into the evolutionary relationships among species and genera, phylogenetic analysis demonstrated two distinct GAB lineages within Venatrix Roewer and Hogna Simon. Population structure analyses of the two most widespread species revealed contrasting patterns. For V. fontis Framenau & Vink, allozyme analyses of 300 individuals at 15 polymorphic loci plus NADH1 sequence analysis of 72 individuals revealed the presence of distinctive subpopulations at most sites, and a partial correlation with overall geographic proximity. In contrast, allozyme analysis of 191 V. arenaris specimens at 12 polymorphic loci demonstrated a comparative lack of both within-site variability and between-site differentiation in the GAB metapopulation.
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Cryptic grey-bellied dunnart (Sminthopsis griseoventer) discovered in South Australia: genetic, morphological and subfossil analyses show the value of collecting voucher material
(C S I R O Publishing, 2011) Kemper, C.; Cooper, S.; Medlin, G.; Adams, M.; Stemmer, D.; Saint, K.; McDowell, G.; Austin, J.
The assumption that almost all mammal species are known to science has led to a recent trend away from collecting voucher specimens/tissues during field studies. Here we present a case study of a recently discovered cryptic marsupial (Sminthopsis griseoventer) in South Australia (SA) and show how such collections can contribute to rigorous biodiversity and biogeographic assessments. Morphological and genetic (allozyme and mitochondrial control region (CR) sequence data) analyses, including ancient DNA analyses of type material, were applied to 188 voucher specimens and 94 non-vouchered tissues of Sminthopsis held at the SA Museum. These data were used to confirm the presence of S. griseoventer in SA, validate means of identifying it morphologically and describe recent and pre-European distributions. Pelage differences between S. griseoventer and S. dolichura enabled their identification, but external measurements overlapped considerably. Subfossil S. griseoventer were identified from seven deposits and confirmed that in the past the species was more widespread in SA. CR divergences (>1.8%) among Western Australian and SA S. griseoventer suggested its long-term presence in SA. Discrepancies between the mitochondrial and allozyme affinities of S. aitkeni and S. griseoventer, coupled with the lack of obvious morphological differences, indicate that a taxonomic reappraisal of these species is warranted. The study strongly demonstrates an ongoing need for the routine collection of mammal voucher material in biological and environmental impact surveys.
Open Access
Desert springs: deep phylogeographic structure in an ancient endemic crustacean (Phreatomerus latipes)
(Public Library of Science, 2012) Guzik, M.; Adams, M.; Murphy, N.; Cooper, S.; Austin, A.; Crandall, K.A.
Desert mound springs of the Great Artesian Basin in central Australia maintain an endemic fauna that have historically been considered ubiquitous throughout all of the springs. Recent studies, however, have shown that several endemic invertebrate species are genetically highly structured and contain previously unrecognised species, suggesting that individuals may be geographically ‘stranded in desert islands’. Here we further tested the generality of this hypothesis by conducting genetic analyses of the obligate aquatic phreatoicid isopod Phreatomerus latipes. Phylogenetic and phylogeographic relationships amongst P. latipes individuals were examined using a multilocus approach comprising allozymes and mtDNA sequence data. From the Lake Eyre region in South Australia we collected data for 476 individuals from 69 springs for the mtDNA gene COI; in addition, allozyme electrophoresis was conducted on 331 individuals from 19 sites for 25 putative loci. Phylogenetic and population genetic analyses showed three major clades in both allozyme and mtDNA data, with a further nine mtDNA sub-clades, largely supported by the allozymes. Generally, each of these sub-clades was concordant with a traditional geographic grouping known as spring complexes. We observed a coalescent time between ~ 2–15 million years ago for haplotypes within each of the nine mtDNA sub-clades, whilst an older total time to coalescence (>15 mya) was observed for the three major clades. Overall we observed that multiple layers of phylogeographic history are exemplified by Phreatomerus, suggesting that major climate events and their impact on the landscape have shaped the observed high levels of diversity and endemism. Our results show that this genus reflects a diverse fauna that existed during the early Miocene and appears to have been regionally restricted. Subsequent aridification events have led to substantial contraction of the original habitat, possibly over repeated Pleistocene ice age cycles, with P. latipes populations becoming restricted in the distribution to desert springs.
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Differential gene flow of mitochondrial and nuclear DNA markers among chromosomal races of Australian morabine grasshoppers (Vandiemenella, viatica species group)
(Blackwell Publishing Ltd, 2007) Kawakami, T.; Butlin, R.; Adams, M.; Saint, K.; Paull, D.; Cooper, S.
Recent theoretical developments have led to a renewed interest in the potential role of chromosomal rearrangements in speciation. Australian morabine grasshoppers (genus Vandiemenella, viatica species group) provide an excellent study system to test this potential role of chromosomal rearrangements because they show extensive chromosomal variation and formed the basis of a classic chromosomal speciation model. There are three chromosomal races, viatica19, viatica17, and P24(XY), on Kangaroo Island, South Australia, forming five parapatric populations with four putative contact zones among them. We investigate the extent to which chromosomal variation among these populations may be associated with barriers to gene flow. Population genetic and phylogeographical analyses using 15 variable allozyme loci and the elongation factor-1alpha (EF-1alpha) gene indicate that the three races represent genetically distinct taxa. In contrast, analyses of the mitochondrial cytochrome c oxidase subunit I (COI) gene show the presence of three distinctive and geographically localized groups that do not correspond with the distribution of the chromosomal races. These discordant population genetic patterns are likely to result from introgressive hybridization between the chromosomal races and range expansions/contractions. Overall, these results suggest that reduction of nuclear gene flow may be associated with chromosomal variation, or underlying genetic variation linked with chromosomal variation, whereas mitochondrial gene flow appears to be independent of this variation in these morabine grasshoppers. The identification of an intact contact zone between P24(XY) and viatica17 offers considerable potential for further investigation of molecular mechanisms that maintain distinct nuclear genomes among the chromosomal races.
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DNA barcoding of stygofauna uncovers cryptic amphipod diversity in a calcrete aquifer in Western Australia's arid zone
(Blackwell Publishing Ltd, 2010) Bradford, T.; Adams, M.; Humphreys, W.; Austin, A.; Cooper, J.
The arid Yilgarn region of Western Australia contains numerous subterranean calcrete aquifers with unique assemblages of obligate groundwater invertebrates (stygofauna). We aimed to establish a DNA barcoding framework for the macro-invertebrates present in a single calcrete, as a basis for future assessment of biodiversity of the Yilgarn calcretes and for investigating food webs. Intense sampling of a bore field grid in the Sturt Meadows calcrete was undertaken to obtain representatives of the entire macro-invertebrate ecosystem. A 623-bp fragment of the mitochondrial cytochrome c oxidase 1 (COI) gene was used to provide DNA barcodes for stygobiont macro-invertebrates plus terrestrial organisms that are found in the calcrete. Phylogenetic analyses revealed the existence of 12 divergent monophyletic groups of haplotypes. Subterranean amphipods (Chiltoniidae) showed three groups of COI haplotypes with sequence divergences between them of >11%. Allozyme analyses found a large number of fixed allelic differences between these three amphipod groups, indicating that there are three morphologically cryptic species within the Sturt Meadows calcrete. Unlike the sister triplet of dytiscid beetles present, the amphipods are not sister clades and are more closely related to other Yilgarn and non-Yilgarn amphipods than to each other. Our results show that the aquifer contains at least 12 macro-invertebrate species and DNA barcoding provides a useful means for discriminating species in this system.
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Genetic analysis of a chromosomal hybrid zone in the Australian Morabine grasshoppers (Vandiemenella, Viatica species group)
(Soc Study Evolution, 2009) Kawakami, T.; Butlin, R.; Adams, M.; Paull, D.; Cooper, S.
Whether chromosomal rearrangements promote speciation by providing barriers to gene exchange between populations is one of the long-standing debates in evolutionary biology. This question can be addressed by studying patterns of gene flow and selection in hybrid zones between chromosomally diverse taxa. Here we present results of the first study of the genetic structure of a hybrid zone between chromosomal races of morabine grasshoppers Vandiemenella viatica, P24(XY) and viatica17, on Kangaroo Island, Australia. Chromosomal and 11 nuclear markers revealed a narrow hybrid zone with strong linkage disequilibrium and heterozygote deficits, most likely maintained by a balance between dispersal and selection. Widths and positions of clines for these markers are concordant and coincident, suggesting that selection is unlikely to be concentrated on a few chromosomes. In contrast, a mitochondrial marker showed a significantly wider cline with centre offset toward the P24(XY) side. We argue that the discordance between the mitochondrial and nuclear/chromosomal clines and overall asymmetry of the clines suggest a secondary origin of the contact zone and potential movement of the zone after contact. Genome-wide scans using many genetic markers and chromosomal mapping of these markers are needed to investigate whether chromosomal differences directly reduce gene flow after secondary contact.
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Genetic elucidation of cryptic and ancient diversity in a group of Australian diplodactyline geckos: The Diplodactylus vittatus complex
(Academic Press Inc Elsevier Science, 2007) Oliver, P.; Hugall, A.; Adams, M.; Cooper, S.; Hutchinson, M.
We examine species boundaries and phylogenetic relationships within the Australian diplodactyline geckos currently assigned to Diplodactylus granariensis and Diplodactylus vittatus using data from multiple allozyme loci, the mitochondrial ND2 gene and published karyotypic studies. These analyses uncover at least six morphologically cryptic but genetically distinctive species. The taxa identified correspond poorly with the existing taxonomy and represent a paraphyletic assemblage with respect to a number of other Diplodactylus species included in analyses. Molecular dating indicates that the species identified evolved considerably before the Pleistocene, and that the basal node of the D. vittatus species group (as redefined here) is of comparable age to entire radiations of other Australian squamate families. The antiquity of this one small group within the diplodactyline geckos suggests that further study of patterns of diversification in the diplodactylines will provide both a valuable insight into long-term patterns of environmental change in the Australian continent and a useful contrast for analysis of patterns of radiation in other Australian lizard groups.
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Great Artesian Basin mound springs reveal cryptic species in the ancient isopod Phreatomerus latipes
(Entomlogical Society, 2009) Guzik, M.; Adams, M.; Murphy, N.; Cooper, S.; Austin, A.; Combined Australian Entomlogical Society AGM (40th : 2009 : Darwin, Australia)
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Independent colonization and extensive cryptic speciation of freshwater amphipods in the isolated groundwater springs of Australia's Great Artesian Basin
(Blackwell Publishing Ltd, 2009) Murphy, N.; Adams, M.; Austin, A.
The groundwater-dependent springs of the Great Artesian Basin (GAB) in arid inland Australia represent a unique and threatened ecosystem. These incredibly isolated springs support a diverse array of endemic flora and fauna. One of the common faunal groups in the GAB springs is the freshwater amphipods of the family Chiltoniidae. The morphological conservatism and taxonomic uncertainty associated with these amphipods has ensured their true biodiversity, phylogeographical history and evolutionary affinities have remained unknown. We have used mitochondrial DNA and allozyme data to unravel a complicated history of isolation, extinction and dispersal among spring amphipod populations across the GAB. The results provide evidence for multiple independent colonizations in the GAB springs, particularly within the Lake Eyre group of springs. The inclusion of a group of Western Australian (WA) stygobitic amphipods from populations up to 1500 km away found surprising evidence for a shared evolutionary history between stygobitic and GAB spring amphipods. Approximate dating of the diversity found between major clades suggests the majority of lineages originated in the late Miocene, around the time of the aridification of inland Australia. The large number of independent lineages and the close connection between GAB spring and WA stygobitic amphipods suggest that a significantly rich amphipod fauna existed in the much wetter environment that once existed in inland Australia. The results also provide evidence for a gross underestimation of the species diversity within the springs, with 12 putative species identified, a conclusion with significant implications for the ongoing conservation of the GAB springs.
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Morphological and electrophoretic taxonomy of the Australian eucalypt leaf-blister sawfly genus Phylacteophaga (Hymenoptera: Pergidae): a potential major pest group of eucalypts worldwide
(CABI Pub., 1997) Mayo, G.; Austin, A.; Adams, M.
The taxonomic status of Phylacteophaga Froggatt is re-evaluated using the independent techniques of allozyme electrophoresis and detailed morphological comparison. Analysis of 45 scorable loci showed highly significant fixed differences (46–51%) among two currently recognized subspecies, P. eucalypti eucalypti Froggatt P. e. froggatti Riek, and a previously unrecognized taxon from Tasmania, demonstrating that they are different species. In addition to colour, significant variation is revealed among P. e. occidens Benson, P. rubida Riek and the three electrophoretically defined species, in body size, structure of the antennae, the shape of the crest, dorsal spines and saw teeth of the ovipositor, and in male genitalia. Based on these results there is substantial justification in recognizing P. occidens and P. rubida as separate species, distinct from P. eucalypti, P. froggatti, and P. amygdalini sp. n. Further, comparison of the holotype of P. e. tasmanica Riek shows it to be conspecific with the lectotype of P. eucalypti (designated here) so that the former species is considered a junior synonym. The distribution of P. eucalypti and P. froggatti is extended to include Tasmania, and a key is presented to distinguish the males and females of all five species. The biology and host plant relations of the species concerned are discussed, along with their pest status and potential to spread to other regions of the world where eucalypts are grown.
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Phylogeography of cave pseudoscorpions in southern Australia
(Blackwell Science Ltd, 2007) Moulds, T.; Murphy, N.; Adams, M.; Reardon, T.; Harvey, M.; Jennings, J.; Austin, A.
Aim To investigate molecular phylogenetic divergence and historical biogeography of the cave-dwelling pseudoscorpion genus Protochelifer. Location Caves and nearby epigean habitats in southern Australia were sampled from western Victoria, Naracoorte Caves, Flinders Ranges, Kangaroo Island, Nullarbor Plain and south-west Western Australia. Methods Allozyme electrophoresis (57 individuals) and a 569-base-pair section of the mtDNA COI gene (22 individuals) were used to reconstruct phylogenetic relationships among four cave species and three epigean species from 13 locations. Results Phylogenetic reconstruction using the allozyme and mtDNA sequence data revealed a similar topology, showing recent speciation of several Protochelifer populations in caves from Naracoorte to the Nullarbor Plain. Naracoorte Caves contained a single species, Protochelifer naracoortensis, found in four separate caves, while all other cave species appear to be restricted to single caves. Main conclusions At a local scale, as indicated by the four Naracoorte caves, dispersal is thought to occur via micro- and mesocaverns, and possibly by phoresy using insect or bat vectors. With current data we are unable to determine if cavernicolous species of Protochelifer have arisen from a single cave colonization event followed by phoretic dispersal on bats to other caves, or multiple cave-invasion events from independent epigean ancestors. Genetic heterogeneity among Protochelifer populations from Nullarbor caves suggest that P. cavernarum, the only species presently recorded from this region, is likely to constitute a species complex requiring further study to fully resolve its relationships.
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Re-examination of a proposed case of stasipatric speciation: phylogeography of the Australian morabine grasshoppers (Vandiemenella viatica species group)
(Blackwell Publishing Ltd, 2009) Kawakami, T.; Butlin, R.; Adams, M.; Saint, K.; Paull, D.; Cooper, S.
Karyotypic differences have been used for delimiting populations or species, although whether these mutations provide strong barriers to gene flow between populations and promote speciation remains contentious. In this study, we assessed whether 11 chromosomal races of Australian morabine grasshoppers (Vandiemenella viatica species group) represent genetically distinct populations by analyses of cytological and allozyme (35 loci) data and DNA sequences of the elongation factor-1 alpha (EF-1alpha), anonymous Mvia11, and mitochondrial cytochrome c oxidase subunit I (COI) loci. While the Vandiemenella chromosomal taxa generally represent genetically distinct units, a substantial portion of the total genetic variation in our samples was not explained by the chromosomal variation. Mantel tests indicated that Vandiemenella populations were spatially structured and have maintained gene flow at a local scale within each of the taxa. The group was subdivided into 13 genetic clusters; four chromosomal taxa comprised single exclusive clusters, while others comprised more than one cluster or clusters shared with other taxa. Boundaries of these cryptic population subdivisions correspond with several biogeographical barriers, such as straits, gulfs, the Murray River, and an ancient mega-lake, Lake Bungunnia. The viatica species group was previously proposed to have diversified without major geographical separation based on the stasipatric speciation model; however, the present study suggests the involvement of allopatric fragmentation. Given extensive nonmonophyly of chromosomal taxa and incomplete barriers to gene flow among taxa, all Vandiemenella chromosomal taxa and genetically distinct populations within chromosomal taxa, except Vandiemenella pichirichi, should be regarded as populations of one species: Vandiemenella viatica.
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The systematics and biology of the spider genus Nephila (Araneae : Nephilidae) in the Australasian region
(C S I R O Publishing, 2007) Harvey, M.; Austin, A.; Adams, M.
Five species of the nephilid genus Nephila Leach are found in the Australasian region, which for the purposes of this study was defined as Australia and its dependencies (including Lord Howe I., Norfolk I., Christmas I., Cocos (Keeling) Is), New Guinea (including Papua New Guinea and the Indonesian province of West Papua), Solomon Is, Vanuatu, New Caledonia, Fiji, Tonga, Niue, New Zealand and other parts of the south-west Pacific region. All species are redescribed and illustrated. Nephila pilipes (Fabricius) occurs in the closed forests of eastern and northern Australia, New Guinea, Solomon Is and Vanuatu (through to South-East Asia); N. plumipes (Latreille) is found in Australia (including Lord Howe I. and Norfolk I.), New Guinea, Vanuatu, Solomon Is and New Caledonia; N. tetragnathoides (Walckenaer) inhabits Fiji, Tonga and Niue; N. antipodiana (Walckenaer) occurs in northern Australia (as well as Christmas I.), New Guinea and Solomon Is (through to South-East Asia); and N. edulis (Labillardière) is found in Australia (including Cocos (Keeling) Is), New Guinea, New Zealand and New Caledonia. Epeira (Nephila) walckenaeri Doleschall, E. (N.) hasseltii Doleschall, N. maculata var. annulipes Thorell, N. maculata jalorensis Simon, N. maculata var. novae-guineae Strand, N. pictithorax Kulczyński, N. maculata var. flavornata Merian, N. pictithorax Kulczyński, N. maculata var. flavornata Merian, N. maculata piscatorum de Vis, and N. (N.) maculata var. lauterbachi Dahl are proposed as new synonyms of N. pilipes. Nephila imperialis var. novaemecklenburgiae Strand, N. ambigua Kulczyński, N. sarasinorum Merian and N. celebesiana Strand are proposed as new synonyms of N. antipodiana. Meta aerea Hogg, N. meridionalis Hogg, N. adelaidensis Hogg and N. meridionalis hermitis Hogg are proposed as new synonyms of N. edulis. Nephila picta Rainbow is removed from the synonymy of N. plumipes and treated as a synonym of N. edulis, and N. nigritarsis insulicola Pocock is removed from the synonymy of N. plumipes and treated as a synonym of N. antipodiana. Allozyme data demonstrate that N. pilipes is distinct at the 80% FD level from N. edulis, N. plumipes and N. tetragnathoides. Nephila plumipes and N. tetragnathoides, deemed to represent sister-taxa owing to the shared presence of a triangular protrusion of the male pedipalpal conductor, were found to differ at 15% FD in the genetic study. No genetic differentiation was found between 10 populations of N. edulis sampled across mainland Australia. Species of the genus Nephila have been extensively used in ecological and behavioural studies, and the biology of Nephila species in the Australasian region is extensively reviewed and compared with studies on Nephila species from other regions of the world.

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