Joel Anthony Huey

High levels of genetic structure in the Australian freshwater fish, Ambassis macleayi

Abstract The genetic structure of the freshwater fish Ambassis macleayi Castelnau 1878 was explored across the tropical catchments of the Gulf of Carpentaria Basin, northern Australia. The Gulf of Carpentaria provides a unique opportunity to explore simultaneously contemporary and historical gene flow resulting from unique climatic patterns and historical connectivity among catchments via a freshwater lake that existed during lower sea levels. The control region of the mtDNA genome and 4 microsatellite loci were used to detect significant genetic structure among and within catchments. Within catchments, genetic structure suggested that dispersal of A. macleayi is restricted, despite high levels of connectivity during summer monsoonal events. Among catchments, divergence appeared to be deeper than what would be predicted based on the last opportunity for connectivity via the lake of Carpentaria (∼10,000 years before present [ybp]). Overall, these results have important implications for A. macleayi and other members of this genus. If individuals are not proficient dispersers, recolonization after disturbance will be limited. Because of historical isolation among catchments, each catchment harbors unique genetic diversity that should be conserved independently.

Low interbasin connectivity in a facultatively diadromous fish: evidence from genetics and otolith chemistry.

Southern smelts (Retropinna spp.) in coastal rivers of Australia are facultatively diadromous, with populations potentially containing individuals with diadromous or wholly freshwater life histories. The presence of diadromous individuals is expected to reduce genetic structuring between river basins due to larval dispersal via the sea. We use otolith chemistry to distinguish between diadromous and nondiadromous life histories and population genetics to examine interbasin connectivity resulting from diadromy. Otolith strontium isotope (87Sr:86Sr) transects identified three main life history patterns: amphidromy, freshwater residency and estuarine/marine residency. Despite the potential for interbasin connectivity via larval mixing in the marine environment, we found unprecedented levels of genetic structure for an amphidromous species. Strong hierarchical structure along putative taxonomic boundaries was detected, along with highly structured populations within groups using microsatellites (FST = 0.046–0.181), and mtDNA (ΦST = 0.498–0.816). The presence of strong genetic subdivision, despite the fact that many individuals reside in saline water during their early life history, appears incongruous. However, analysis of multielemental signatures in the otolith cores of diadromous fish revealed strong discrimination between river basins, suggesting that diadromous fish spend their early lives within chemically distinct estuaries rather than the more homogenous marine environment, thus avoiding dispersal and maintaining genetic structure.

Migration history and stock structure of two putatively diadromous teleost fishes, as determined by genetic and otolith chemistry analyses

Abstract: n Migratory life cycles and population structure of 2 putatively diadromous Australian fishes were examined using otolith chemistry (87Sr/86Sr) and genetics (microsatellites and mitochondrial deoxyribonucleic acid [mtDNA]). Australian whitebait (Lovettia sealii) is widely considered to be one of only a few anadromous fish species in the southern hemisphere. The congolli or tupong (Pseudaphritis urvillii) is reported to undertake an unusual form of sexually segregated catadromous migration, where females switch habitats between marine and freshwater, while males remain in marine or estuarine environments. Sr-isotope profiles of L. sealii showed this species does not move into fully freshwater habitats during its life cycle, suggesting it should be considered semianadromous or estuarine-dependent, rather than truly anadromous. This life-history strategy is unique among the Galaxiidae. Lovettia sealii is regionally divided into at least 3 well differentiated genetic stocks: northern and southern Tasmanian coasts and mainland Australia. Sr-isotope profiles of P. urvillii showed that females are catadromous, with the early life history spent in the marine environment and a single migratory transition from marine to freshwater occurring at an early point in the life history. Lack of bidirectional adult migration between freshwater and the sea suggests that female P. urvillii are semelparous, returning to the marine habitat to mate with resident males after an extended period of freshwater residence. Pseudaphritis exhibit weak genetic structure across their mainland range. An isolation-by-distance relationship describes the genetic structure of this species, a pattern it shares with several other nearshore-restricted catadromous fishes.

Extremely Low Microsatellite Diversity but Distinct Population Structure in a Long-Lived Threatened Species, the Australian Lungfish Neoceratodus forsteri (Dipnoi)

The Australian lungfish is a unique living representative of an ancient dipnoan lineage, listed as ‘vulnerable’ to extinction under Australia’s Environment Protection and Biodiversity Conservation Act 1999. Historical accounts indicate this species occurred naturally in two adjacent river systems in Australia, the Burnett and Mary. Current day populations in other rivers are thought to have arisen by translocation from these source populations. Early genetic work detected very little variation and so had limited power to answer questions relevant for management including how genetic variation is partitioned within and among sub-populations. In this study, we use newly developed microsatellite markers to examine samples from the Burnett and Mary Rivers, as well as from two populations thought to be of translocated origin, Brisbane and North Pine. We test whether there is significant genetic structure among and within river drainages; assign putatively translocated populations to potential source populations; and estimate effective population sizes. Eleven polymorphic microsatellite loci genotyped in 218 individuals gave an average within-population heterozygosity of 0.39 which is low relative to other threatened taxa and for freshwater fishes in general. Based on F ST values (average over loci = 0.11) and STRUCTURE analyses, we identify three distinct populations in the natural range, one in the Burnett and two distinct populations in the Mary. These analyses also support the hypothesis that the Mary River is the likely source of translocated populations in the Brisbane and North Pine rivers, which agrees with historical published records of a translocation event giving rise to these populations. We were unable to obtain bounded estimates of effective population size, as we have too few genotype combinations, although point estimates were low, ranging from 29 - 129. We recommend that, in order to preserve any local adaptation in the three distinct populations that they be managed separately.

Broadscale phylogeographic structure of five freshwater fishes across the Australian Monsoonal Tropics

Abstract: n The Australian Monsoonal Tropics (AMT) is a unique location for the study of phylogeography and intraspecific genetic variation in freshwater fish. We assessed the phylogeographic structure of 5 species from 2 genera across the region. The species included 3 neosilurids (Plotosidae, Neosilurus hyrtlii, Neosilurus ater, and Neosilurus pseudospinosus) and 2 members of the genus Oxyeleotris (Eleotridae, O. selheimi and O. lineolata). We used mitochondrial deoxyribonucleic acid (mtDNA) and phylogenetic analyses to explore the phylogeographic histories of these species. Overall, phylogeographic patterns were inconsistent. Some species were highly structured, and phylogeographic breaks were detected (e.g., N. hyrtlii, N. pseudospinosus, and O. selheimi), but other species showed no obvious divergences across the AMT (N. ater and O. lineolata). All species sampled in the Gulf of Carpentaria had shallow phylogenies, consistent with the expectation that historically, Lake Carpentaria would have provided connectivity through this region. All species also showed evidence of recent connectivity across drainage divides on the eastern and western coasts of the Cape York Peninsula. Some species in the Kimberley region were highly structured, consistent with expectation that these ancient and geologically stable catchments would promote divergence in allopatry. Conservation efforts should now be directed toward ensuring that the intraspecific biodiversity identified in our study and others are protected in the future.

Natural and anthropogenic drivers of genetic structure and low genetic variation in the endangered freshwater cod, Maccullochella mariensis

Population genetic theory has identified several threats to small populations that have the potential to endanger species in the short and long term. Understanding these threats is particularly pertinent when management actions, such as stocking, have the potential to exacerbate them. In this study we explore existing genetic variation in the threatened Mary River Cod, Maccullochella mariensis, which has had a long stocking history in its endemic populations (Mary River and Tinana–Coondoo Creek) and has been translocated into other catchments in Southeast Queensland (SEQ). Using Bayesian clustering analysis, two genetically distinct sub-populations were detected (Mary and SEQ vs. Tinana–Coondoo), despite decades of stocking from one population (Tinana–Coondoo) into the other (Mary). Overall, genetic diversity (1–9 alleles per locus) and Ne (18–56)xa0were low, but bigger in the Mary, relative to Tinana–Coondoo. Interestingly, evidence for historical unidirectional gene flow from Tinana–Coondoo into the Mary was detected, which was not as strongly reflected using contemporary estimators, suggesting stocking has not dramatically altered the existing genetic structure for this species. These results provide an opportunity for managers to strategically design stocking protocols and to improve the condition of this species in the wild.

Aquatic Insects in Eastern Australia: A Window on Ecology and Evolution of Dispersal in Streams.

Studies of connectivity of natural populations are often conducted at different timescales. Studies that focus on contemporary timescales ask questions about dispersal abilities and dispersal behavior of their study species. In contrast, studies conducted at historical timescales are usually more focused on evolutionary or biogeographic questions. In this paper we present a synthesis of connectivity studies that have addressed both these timescales in Australian Trichoptera and Ephemeroptera. We conclude that: (1) For both groups, the major mechanism of dispersal is by adult flight, with larval drift playing a very minor role and with unusual patterns of genetic structure at fine scales explained by the “patchy recruitment hypothesis”; (2) There is some evidence presented to suggest that at slightly larger spatial scales (∼100 km) caddisflies may be slightly more connected than mayflies; (3) Examinations of three species at historical timescales showed that, in southeast Queensland Australia, despite there being no significant glaciation during the Pleistocene, there are clear impacts of Pleistocene climate changes on their genetic structure; and (4) The use of mitochondrial DNA sequence data has uncovered a number of cryptic species complexes in both trichopterans and ephemeropterans. We conclude with a number of suggestions for further work.

The linking of plate tectonics and evolutionary divergence.

It is exciting to be living at a time when the big questions in biology can be investigated using modern genetics and computing [1]. Bauza-Ribot et al.[2] take on one of the fundamental drivers of biodiversity, the effect of continental drift in the formation of the world’s biota 3 and 4, employing next-generation sequencing of whole mitochondrial genomes and modern Bayesian relaxed molecular clock analysis. Bauza-Ribot et al.[2] conclude that vicariance via plate tectonics best explains the genetic divergence between subterranean metacrangonyctid amphipods currently found on islands separated by the Atlantic Ocean. This finding is a big deal in biogeography, and science generally [3], as many other presumed biotic tectonic divergences have been explained as probably due to more recent transoceanic dispersal events [4]. However, molecular clocks can be problematic 5 and 6 and we have identified three issues with the analyses of Bauza-Ribot et al.[2] that cast serious doubt on their results and conclusions. When we reanalyzed their mitochondrial data and attempted to account for problems with calibration 5 and 6, modeling rates across branches 5 and 7 and substitution saturation [5], we inferred a much younger date for their key node. This implies either a later trans-Atlantic dispersal of these crustaceans, or more likely a series of later invasions of freshwaters from a common marine ancestor, but either way probably not ancient tectonic plate movements.

Did common disjunct populations of freshwater fishes in northern Australia form from the same biogeographic events

Abstract: n Several freshwater fishes have disjunct (geographically discrete and widely spaced) distributions across northern Australia. We used mitochondrial deoxyribonucleic acid (mtDNA) data and phylogeographic analyses to examine the origin of these common disjunct distributions and to test the hypothesis that they were a result of a single biogeographic event. These disjunct distributions are not perfectly shared among species, but we selected 3 species that have wide ranges with the most similar disjunct geographic overlap: Spotted Blue Eye (Pseudomugil gertrudae), Pennyfish (Denariusa australis), and MacCullochs Rainbow Fish (Melanotaenia maccullochi). Despite similarity in their present-day disjunct distributions, spatial genetic patterns varied considerably among the 3 species in terms of measures of molecular diversity, number of mtDNA lineages within each species, inter- and intra-regional spatial distribution of individual lineages within species, and degree of partitioning of genetic variation among regions. Pseudomugil gertrudae and D. australis each contained 1 to 2 divergent lineages at particular sites in 1 of the regions (Top End), but both species also contained lineages in this region that were more closely related to conspecific populations in other regions. Two regional populations (Top End and Northern Cape York Peninsula) of M. maccullochi consisted exclusively of highly divergent lineages that probably reflect cryptic species. When the divergent lineages within each species were excluded from temporal analyses, a single vicariant event among regions could not be rejected. Our results indicate that several regional populations are long-term relicts for M. maccullochi and that several sites within Top End are associated with localized long-term refugia for P. gertrudae and D. australis. A single biogeographic event in the mid- to late-Pleistocene may have created broadscale separation of most populations of these species.

Population structure of sexually reproducing carp gudgeons: does a metapopulation offer refuge from sexual parasitism?

Australian carp gudgeons (Hypseleotris spp.) of the Murray–Darling basin are a species complex including sexually reproducing taxa and unisexual hybrid lineages that reproduce via hybridogenesis. Unisexual fish require gametes of a sexual species to propagate themselves and can be regarded as ‘sexual parasites’ capable of driving closed populations to extinction. Metapopulation dynamics have been proposed as a mechanism that could facilitate coexistence between a sexual parasite and its ‘host’. This study evaluates whether patterns of spatial genetic variation are compatible with metapopulation dynamics for a sexually reproducing member of the carp gudgeon complex (Hypseleotris sp. HA), in the Granite Creeks system of central Victoria. Genetic differentiation of fish among all study sites was accommodated by a model of migration-drift equilibrium using decomposed pairwise regression analysis. Given that the population was divided into discrete patches in the form of refugial waterholes during the time of this study, we infer that spatially constrained source–sink metapopulation dynamics may be responsible for producing this pattern. It is therefore possible that metapopulation dynamics contribute to coexistence in the Granite Creeks carp gudgeon hybridogenetic system, and further analysis is required to determine the relative importance of environmental versus demographic factors towards patch extinction.