Obligate Freshwater Fish Research Articles

Long-term climatic stability drives accumulation and maintenance of divergent freshwater fish lineages in a temperate biodiversity hotspot

Anthropogenic climate change is forecast to drive regional climate disruption and instability across the globe. These impacts are likely to be exacerbated within biodiversity hotspots, both due to the greater potential for species loss but also to the possibility that endemic lineages might not have experienced significant climatic variation in the past, limiting their evolutionary potential to respond to rapid climate change. We assessed the role of climatic stability on the accumulation and persistence of lineages in an obligate freshwater fish group endemic to the southwest Western Australia (SWWA) biodiversity hotspot. Using 19,426 genomic (ddRAD-seq) markers and species distribution modelling, we explored the phylogeographic history of western (Nannoperca vittata) and little (Nannoperca pygmaea) pygmy perches, assessing population divergence and phylogenetic relationships, delimiting species and estimating changes in species distributions from the Pliocene to 2100. We identified two deep phylogroups comprising three divergent clusters, which showed no historical connectivity since the Pliocene. We conservatively suggest these represent three isolated species with additional intraspecific structure within one widespread species. All lineages showed long-term patterns of isolation and persistence owing to climatic stability but with significant range contractions likely under future climate change. Our results highlighted the role of climatic stability in allowing the persistence of isolated lineages in the SWWA. This biodiversity hotspot is under compounding threat from ongoing climate change and habitat modification, which may further threaten previously undetected cryptic diversity across the region.

Multi-gene insights into the taxonomy and conservation of Tasmania’s galaxiid fishes

Context Galaxiids are a widespread, southern hemisphere, radiation of mostly obligate freshwater fishes. Tasmania houses a diversity of endemic species of Galaxias and Paragalaxias. Of these, many are at risk of extinction, being landlocked, range-restricted and subject to anthropogenic threats, placing a high-conservation priority on the region. Aim Our aim was to synthesise historic and published molecular datasets to provide the sound systematic framework needed to underpin future conservation and taxonomic efforts for Tasmanian galaxiids. Methods Novel and published nuclear (allozyme) and matrilineal (cytb) datasets were generated and integrated for every putative Tasmanian galaxiid species lacking a comparable multi-gene assessment. Key results The Tasmanian galaxiids are phylogenetically diverse, with molecular data generally supporting the accepted taxonomy, but with potential species-level diversity noted within an alpine radiation of the Galaxias truttaceus complex and further support for synonymy of G. niger within G. brevipinnis. Conclusions This study highlights the value of multi-locus studies in both validating species-level taxonomy and resolving taxonomic ambiguities and conservation priorities within Tasmania’s galaxiids. Implications Our integrated genetic analyses provide a framework to underpin more in-depth genomic approaches to assess additional cryptic diversity and conservation planning, such as genetic rescue and ex situ population security.

Landscape Evolution as a Diversification Driver in Freshwater Fishes

The exceptional concentration of vertebrate diversity in continental freshwaters has been termed the “freshwater fish paradox,” with > 15,000 fish species representing more than 20% of all vertebrate species compressed into tiny fractions of the Earth’s land surface area (<0.5%) or total aquatic habitat volume (<0.001%). This study asks if the fish species richness of the world’s river basins is explainable in terms of river captures using topographic metrics as proxies. The River Capture Hypothesis posits that drainage-network rearrangements have accelerated biotic diversification through their combined effects on dispersal, speciation, and extinction. Yet rates of river capture are poorly constrained at the basin scale worldwide. Here we assess correlations between fish species density (data for 14,953 obligate freshwater fish species) and basin-wide metrics of landscape evolution (data for 3,119 river basins), including: topography (elevation, average relief, slope, drainage area) and climate (average rainfall and air temperature). We assess the results in the context of both static landscapes (e.g., species-area and habitat heterogeneity relationships) and transient landscapes (e.g., river capture, tectonic activity, landscape disequilibrium). We also relax assumptions of functional neutrality of basins (tropical vs. extratropical, tectonically stable vs. active terrains). We found a disproportionate number of freshwater species in large, lowland river basins of tropical South America, Africa, and Southeast Asia, under predictable conditions of large geographic area, tropical climate, low topographic relief, and high habitat volume (i.e., high rainfall rates). However, our results show that these conditions are only necessary, but not fully sufficient, to explain the basins with the highest diversity. Basins with highest diversity are all located on tectonically stable regions, places where river capture is predicted to be most conducive to the formation of high fish species richness over evolutionary timescales. Our results are consistent with predictions of several landscape evolution models, including the River Capture Hypothesis, Mega Capture Hypothesis, and Intermediate Capture Rate Hypothesis, and support conclusions of numerical modeling studies indicating landscape transience as a mechanistic driver of net diversification in riverine and riparian organisms with widespread continental distributions.

Phylogeography of the Cran’s bullyGobiomorphus basalis(Gobiiformes: Eleotridae) and an analysis of species boundaries within the New Zealand radiation ofGobiomorphus

AbstractNew Zealand has a complex recent history of climatic and tectonic change that has left variable signatures in the geographic distribution and genetic structure of the region’s flora and fauna. To identify concordant patterns, a broad range of taxa must be examined and compared. In New Zealand’s North Island, a consensus is forming as to the dominant biogeographic barriers in the region although obligate freshwater taxa have not been considered in this framework. We use single-nucleotide polymorphisms to investigate phylogeography in the widespread obligate freshwater fish Gobiomorphus basalis on the North Island. Phylogeographic patterns within G. basalis reveal biogeographic disjunctions that are in some ways consistent and in other ways at odds with established patterns, providing insight into the processes that have shaped the islands’ biogeography. We also use phylogeography to delineate species boundaries within the entire New Zealand radiation of Gobiomorphus and find that it contains several morphologically cryptic species. We resolve two clades within G. basalis that correspond to areas north and south of the Taupo Volcanic Zone. We confirm the distinctiveness of Gobiomorphus alpinus relative to Gobiomorphus cotidianus, as well as the presence of two lineages within Gobiomorphus breviceps that were previously identified based on mitochondrial data.

Between an ocean and a high place: coastal drainage isolation generates endemic cryptic species in the Cape kurper Sandelia capensis (Anabantiformes: Anabantidae), Cape Region, South Africa.

This study investigated the range-wide phylogenetics and biogeography of the Cape kurper Sandelia capensis, a primary freshwater fish endemic to and widespread within the Cape Floristic Region (CFR) of South Africa. Maximum likelihood, Bayesian phylogenetic and haplotype network analyses, based on two mitochondrial and two nuclear genes, revealed the existence of three reciprocally monophyletic, deeply divergent and allopatric clades that probably represent cryptic species. The West Coast Clade is largely confined to the Langvlei, Verlorenvlei, Berg and Diep Rivers, the Klein River Clade is endemic to the Klein River and the South Coast Clade is found everywhere else in the range of S. capensis sensu lato. It was hypothesised that divergences within S. capensis sensu lato probably occurred because of isolation of coastal drainages by persistent drainage divides or vicariance of current tributaries by the drowning of their confluences by high sea levels. The current distribution of lineages could be due to historical range expansion and gene flow via river capture or some other mode of transdivide dispersal or dispersal during periods of low sea level via palaeoriver confluences of currently isolated coastal rivers. Comparison of BEAST2 estimated divergence times with the timing of climatic, geological and geomorphological events supported long-term coastal drainage isolation, punctuated by rare transdivide dispersal events and limited palaeoriver dispersal, as the best explanation of current phylogeographic and divergence patterns in S. capensis. Hydrological barriers that block upstream passage in palaeotributaries could hypothetically explain why S. capensis failed to disperse through certain palaeoriver confluences. There were several sites where biogeographic patterns have likely been confounded by human translocation of S. capensis. Alien fish predators and water extraction may threaten the three cryptic species more severely than previously realised, due to their smaller population sizes and inhabitation of only a portion of the range previously ascribed to S. capensis sensu lato. The preponderance of cryptic diversity and endemism in the CFR suggests that additional undescribed cryptic species of obligate freshwater fishes may be found in short coastal river systems around the world, especially in regions with a history of geological stability and a narrow continental shelf.

Historical abiotic events or human-aided dispersal: inferring the evolutionary history of a newly discovered galaxiid fish.

Range expansion of obligate freshwater fishes in the Cape Floristic Region (CFR) of South Africa has mostly been attributed to river capture events and confluence of rivers following sea-level regression. The role of low drainage divides and interbasin water transfers has received less attention. This study analyzed mitochondrial and nuclear DNA sequences to assess the processes that could have influenced the phylogeographic patterns of a newly discovered lineage of Galaxias zebratus (hereafter Galaxias zebratus “Joubertina”) that occurs across two currently isolated river systems close to the Joubertina area in the eastern CFR. Results from both analyses revealed that observed genetic differentiation cannot be explained by isolation between the two river systems. No genetic differentiation was found between the Krom River system and a population from one of the Gamtoos tributaries. Shallow genetic differentiation was found between the Krom and the other Gamtoos populations. Historical river capture events and sea-level changes do not explain the present distribution of Galaxias zebratus “Joubertina” across the Krom and Gamtoos River systems. Interbasin dispersal during pluvial periods, recent river capture, or recent human-mediated translocation seems to be the most plausible explanations.

Effect of salinity on growth of juvenile Yarra pygmy perch (Nannoperca obscura: Percichthyidae)

The threatened Yarra pygmy perch (Nannoperca obscura) is an obligate freshwater fish endemic to the south-eastern coast of mainland Australia, where a majority of river systems have been heavily modified since European settlement. The purpose of this garden study was to explore any relationship between the growth rate of juvenile N. obscura with respect to salinity. Trials were conducted encompassing perceived and potential ranges within the species’ environment, through five salinity treatments and recorded growth after 8 weeks. Two brood-groups were trialed simultaneously to observe any intrapopulation variance in phenotypic response potentially linked to genetic variance. The salinity trials found a clear model indicating increasing growth for moderate salinities (i.e. 2.5–7.5 ppt), therefore identifying the ideal salinity range for N. obscura juveniles. Phenotypic response between brood-groups was varied and inconsistent, potentially reflecting low genetic variability. With a limited genetic variance restricting adaptability, tolerance to a changing environment would be reduced. Therefore increased salinization and subsequent flushing events within habitats may be key threats to the species’ survival.

Statistical phylogeographic tests of competing 'Lake Carpentaria hypotheses' in the mouth-brooding freshwater fish, Glossamia aprion (Apogonidae)

Glacial cycles during the Pleistocene reduced sea levels and created new land connections in northern Australia, where many currently isolated rivers also became connected via an extensive paleo-lake system, ‘Lake Carpentaria’. However, the most recent period during which populations of freshwater species were connected by gene flow across Lake Carpentaria is debated: various ‘Lake Carpentaria hypotheses’ have been proposed. Here, we used a statistical phylogeographic approach to assess the timing of past population connectivity across the Carpentaria region in the obligate freshwater fish, Glossamia aprion. Results for this species indicate that the most recent period of genetic exchange across the Carpentaria region coincided with the mid- to late Pleistocene, a result shown previously for other freshwater and diadromous species. Based on these findings and published studies for various freshwater, diadromous and marine species, we propose a set of ‘Lake Carpentaria’ hypotheses to explain past population connectivity in aquatic species: (1) strictly freshwater species had widespread gene flow in the mid- to late Pleistocene before the last glacial maximum; (2) marine species were subdivided into eastern and western populations by land during Pleistocene glacial phases; and (3) past connectivity in diadromous species reflects the relative strength of their marine affinity.

A delineation of Nuclear Middle America biogeographical provinces based on river basin faunistic similarities

The biogeographical patterns of the obligate freshwater fishes of Nuclear Middle America, a region that expands from southern Guatemala to northern Nicaragua, are described herein. Historically, three broad ichthyological provinces have been assigned to Nuclear Middle America: the Usumacinta, and the San Juan in the Atlantic slope and the Chiapas-Nicaraguense in the Pacific slope. With the use of correspondence analysis and unweighted pair group method with arithmetic mean cluster analysis of a presence/absence matrix of 76 obligate freshwater fishes, we identified four ichthyological provinces in Nuclear Middle America: (1) the Honduras and Guatemala Caribbean Highlands Province, (2) the Honduras and Nicaragua Mosquitia Province, (3) the Chiapas-El Salvador-Nacaome Province, and (4) the Choluteca and Nicaragua Pacific Province. Differences between provinces in species composition and species turnover between provinces were tested by analysis of similarity, the calculation of beta-diversity indices and an indicator species analysis. We then further characterized each province by identifying the number of endemics and classifying species according to their salinity tolerance. The most striking patterns of Nuclear Middle America freshwater fish distribution are its paucity of primary freshwater fishes and limited numbers of endemics. The four ichthyological provinces are distinct as indicated by the ANOSIM and beta-diversity analysis, although one province showed low beta-diversity values. These results suggest that, despite of the active geological history that characterized the region, there has been limited isolation of species in any given province, and historical drainage connectivity has been high.

Genetic structure and phylogeography of two freshwater fishes, Rhadinocentrus ornatus and Hypseleotris compressa, in southern Queensland, Australia, inferred from allozymes and mitochondrial DNA

This study used allozyme and mtDNA variation to examine genetic structure in Rhadinocentrus ornatus and Hypseleotris compressa in southern Queensland. The aim of this study was to test the hypothesis that dispersal between coastal streams was greater in R. ornatus than in H. compressa and to test whether R. ornatus would reflect a similar pattern seen in another obligate freshwater fish in the same region, that is, R. ornatus will show genetic homogeneity among streams of the Sunshine Coast but significant differentiation among all other streams. Evidence from the current study suggests that, in R. ornatus, there was significant genetic differentiation among populations within regions, which explains why this species has very restricted dispersal abilities between streams, even between those very close to one another. On the other hand, H. compressa showed very low levels of genetic differentiation suggesting some gene flow among regions by virtue of dispersal. High levels of genetic differentiation were identified between all coastal streams in the area, including those hypothesized to have been recently connected in the Sunshine Coast area in the case of R. ornatus.

Groundwater contribution to baseflow maintains habitat connectivity forTandanus bostocki(Teleostei: Plotosidae) in a south‐western Australian river

Beatty SJ, Morgan DL, McAleer FJ, Ramsay AR. Groundwater contribution to baseflow maintains habitat connectivity forTandanus bostocki(Teleostei: Plotosidae) in a south‐western Australian river. Ecology of Freshwater Fish 2010: 19: 595–608. © 2010 John Wiley & Sons A/SAbstract – A global biodiversity hotspot, south‐western Australia is characterised by a highly endemic freshwater fish fauna that is severely impacted by habitat alterations. As is the case with many rivers in this region, the Blackwood River is secondarily salinised as a consequence of agricultural practices and this has caused population depletions of halo‐intolerant fishes. This study is the first to examine the role that groundwater intrusion has in maintaining habitat connectivity for an obligate freshwater fish in a secondarily salinised river. We determined the significance of nonsaline groundwater intrusion in maintaining habitat and migratory routes of the freshwater cobbler,Tandanus bostockiduring prolonged annual dry periods; characteristic of Mediterranean climatic zones.Tandanus bostockiundertook large, yet spatially and temporally variable, localised movements through riffles. During baseflow, the period of major groundwater influence, movements were significantly associated with discharge. Analysis of gonadal development suggested that such movements were not strictly related to reproduction and were probably for foraging purposes. The study reveals groundwater is crucial in maintaining migratory routes through riffles and suggestsT. bostockimay be reliably used as an indicator of aquatic habitat connectivity in light of groundwater extractions and also continued rainfall reductions in this region due to climate change.

Impact of ocean barriers, topography, and glaciation on the phylogeography of the catfish Trichomycterus areolatus (Teleostei: Trichomycteridae) in Chile

We examined the role of several earth history events on the phylogeographic distribution of the catfish Trichomycterus areolatus in Chile using the cytochrome b gene. We explored three biogeographic hypotheses: that sea level changes have resulted in the isolation of populations by drainages; that glaciation has impacted genetic diversity; and that ichthyological subprovince boundaries correspond to phylogeographic breaks in our focal species. We found seven well-supported clades within T. areolatus with high levels of genetic divergence. The strongest signal in our data was for an important role of sea level changes structuring populations. Five of the seven clades mapped cleanly to the geographic landscape and breaks corresponded closely to areas of narrowest continental shelf. In addition, few haplotypes were shared between rivers within clades, suggesting that only limited local movement of individuals has occurred. There was no relationship between the levels of genetic diversity and the proportion of individual drainages covered by glaciers during the last glacial maximum. Two phylogeographic breaks within T. areolatus did match the two previously identified faunal boundaries, but we found three additional breaks, which suggests that faunal breaks have only limited utility in explaining phylogeographic patterns. These results imply that the narrow continental shelf coupled with sea level changes had a strong influence on the obligate freshwater fishes in Chile.

Late glacial impacts on dispersal and colonization of Atlantic Canada and Maine by freshwater fishes

Late glacial scenarios of ice retreat and biogeography databases constrain the dispersal routes of obligate freshwater fishes into Atlantic Canada and Maine. Evidence indicates glacial ice covered the present-day mainland and offshore islands at 18,000 14C yr before present. Possible refugia for extirpated freshwater fishes were the exposed outer edge of the Grand Banks (east), exposed Georges Bank (south-Atlantic Refugium), and the Mississippi Refugium in the west. It is improbable that the region was recolonized from the offshore refugia. Rather, fishes recolonized from the east via the upper St. Lawrence River valley into the upper Saint John River, Maine (Lake Madawaska) from 11,000 to 12,000 14C yr BP. The short period of entry resulted in the low diversity of obligate freshwater species in the region. Lake Madawaska was breached and dispersal continued into the remainder of the region after 8000 14C yr BP. By 6000 14C yr BP, access routes to the east along low-lying coastal zones were blocked by rising sea levels, which isolated Prince Edward Island, Cape Breton Island, and most probably Nova Scotia. Natural dispersal across the region appeared complete by this time.

Historical biogeography of South American freshwater fishes

AbstractAim To investigate biogeographical patterns of the obligate freshwater fish order Characiformes.Location South America.Methods Parsimony analysis of endemicity, likelihood analysis of congruent geographical distribution, and partition Bremer support were used.Results Areas of endemism are deduced from parsimony analysis of endemicity, and putative dispersal routes from a separate analysis of discordant patterns of distribution.Main conclusions Our results demonstrate the occurrence of 11 major areas of endemism and support a preferential eastern–western differentiation of the characiforms in the Amazonian region, contrasting with the southern–northern differentiation of terrestrial organisms. The areas of endemism identified seem to be deeply influenced by the distribution of the emerged land during the 100‐m marine highstand that occurred during the late Miocene and allow us to hypothesize the existence of eight aquatic freshwater refuges at that time. The raw distribution of non‐endemic species supports nine patterns of species distribution across the 11 areas of endemism, two of which support a southern–northern differentiation in the eastern part of the Amazon. This result shows that the main channel of the Amazon limited dispersal between tributaries from each bank of the river. The levels of endemism further demonstrate that the aquatic freshwater refuges promoted allopatric speciation and later allowed the colonization of the lowlands. By contrast, the biogeographical pattern found in the western part of the Amazon is identified as a result of the Miocene Andean foreland dynamic and the uplift of the palaeoarches that promoted allopatric divergence across several sedimentary basins by the establishment of disconnected floodplains. The assessment of conflicting species distributions also shows the presence of seven putative dispersal routes between the Amazon, Orinoco and Paraná rivers. Our findings suggest that, rather than there being a single predominant process, the establishment of the modern South American freshwater fish biotas is the result of an interaction between marine incursions, uplift of the palaeoarches, and historical connections allowing cross‐drainage dispersal.

The impact of postglacial marine invasions on the genetic diversity of an obligate freshwater fish, the longnose dace (Rhinichthys cataractae), on the Quebec peninsula

Postglacial seas are expected to have had significant effects on the genetic structure of populations of obligate freshwater fishes. To assess this influence, mitochondrial DNA variability was evaluated in 32 populations of longnose dace (Rhinichthys cataractae) of the Quebec peninsula located within and outside of the maximum extent of marine invasions of the Champlain and Laflamme seas. Three clades of haplotypes diverging from one to two mutations were defined. Despite this low divergence, a clear and significant spatial genetic structure was observed outside of the extent of marine invasions. However, a higher genetic diversity was observed in populations located within the extent of marine invasions because of the admixture of these clades with an additional lineage restricted almost exclusively to those areas. The low genetic divergence between the main haplotypes suggests a single origin, despite the known presence of this species in various refuges. Marine invasions preventing entry to the peninsula, especially from Atlantic refuge, are proposed as a possible explanation to this particular result. This study is a relevant argument for integrating postglacial marine invasions into postglacial colonization models of freshwater species in the northeastern part of North America.

Maximum Ages of Ciliate Lineages Estimated Using a Small Subunit rRNA Molecular Clock: Crown Eukaryotes Date Back to the Paleoproterozoic

Summary We estimated the rate of nucleotide substitution for the obligate freshwater fish ectoparasite, Ichthyophthirius , and its closest free-living relative, Ophryoglena , using an independently-timed event — the origin of freshwater fish in the fossil record. Based on this information, the rate of nucleotide substitution per site, per year, per lineage is 1.25 to 1.4 × 10 −8 or 1% divergence per 72 to 80 million years (My). Using this rate, we determined that the origin of the ciliates (i.e. crown eukaryotes) is much older than previously speculated, dating back to the Paleoproterozoic some 1980 to 2200 million years ago (Ma). We also determined that the wellestablished lineages recognized as classes today (e.g. Spirotrichea, Oligohymenophorea, Nassophorea, Colpodea, Heterotrichea, Karyorelictea, and Litostomatea) diverged within 600-My of the ciliate-like ancestor diverging from the main eukaryotic line.

Phylogeographic structure in mitochondrial DNA of a South‐east Asian freshwater fish, Hemibagrus nemurus (Siluroidei; Bagridae) and Pleistocene sea‐level changes on the Sunda shelf

AbstractWe postulated that the biogeographical history of South‐east Asia contributed to extensive admixture during Pleistocene low sea levels of genetic groups of an obligate freshwater fish (the river catfish, Hemibagrus nemurus) isolated during periods of high sea levels. During Pleistocene glacial maxima, the sea level was lower than at present and the islands of the Sunda shelf (Sumatra, Borneo and Java) and the Asian mainland were connected by lowlands traversed by rivers. Restriction fragment length polymorphisms in mitochondrial DNA were documented for 140 putative H. nemurus analysed from 13 sampling sites resulting in the definition of 35 haplotypes. The high level of haplotype differentiation (mean P × 100 = 2.22, SD = 1.33) indicates that the subdivision of the ancestral H. netnurus group was extensive and probably occurred early in the Pleistocene. The occurrence of some genetically divergent groups of the H. netnurus complex occurring in sympatry in widely separated locations supports the proposition that low sea levels aided the dispersion and mingling of genetic groups. Based on both genetic and morphological evidence, the main H. nemurus line gave rise to three regional groups: (1) a morphologically distinct ‘Indochinese’ group composed of two mtDNA clades overlapping in east peninsular Malaysia; (2) a ‘Sundaic’ group composed of various lineages of differing morphology and genetic identity; (3) a genetically distinct ‘Sarawak’ group in west Borneo, similar in morphology to the ‘Sundaic’ and ‘Indochinese’ groups, but including a small, golden colour morph as a distinct dade. The morphologically similar Sundaic forms from west Java, Sumatra and west Borneo show some degree of genetic divergence, but their phylogenetic relationships are poorly resolved. The most genetically and morphologically distinct Sundaic dade, assigned to H. hoevenii, colonized the Kapuas river (west Borneo), east Sumatra and south peninsular Malaysia. Contrary to our original hypothesis and present biogeographical theory, little exchange of genetic groups has apparently occurred between the mainland and the Sunda Islands during recent glaciations.