Phylogeography and ecological speciation of fishes

Ecological speciation results from divergent natural selection acting on adaptive traits responsible for reproductive isolation. Recent studies have shown that the evolution of reproductive isolation and niche divergence during ecological speciation can take place fast and in the presence of gene flow (i.e. in the absence of physical barriers). Phylogeography provides a valuable framework for assessing the existence of allopatric phases during speciation and, as a result, improves our ability to identify signatures of divergent natural selection associated with ecological divergence.

We study ecological speciation and phylogeography of freshwater and marine fishes from the Pampas, Patagonia, Amazonia, Gulf of California and Australia. We have developed projects on teleosts and elasmobranchs impacted by divergences dating from the Holocene to the Tertiary. Despite the variety of scenarios and species targeted by our projects, our focus is on incipient ecological species – these present an opportunity to investigate ongoing evolutionary processes in scenarios where adaptive divergence and reproductive isolation are closely associated.

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Research projects

– Isolation by Adaptation and Sea Level Changes in Silverside Fishes from the Pampas and Patagonia
We were arguably the first to describe a scenario of fish speciation in South America driven by divergent natural selection. We showed that niche divergence due to estuarine colonization by marine silverside fish (genus Odontesthes) led to isolation by adaptation and speciation in the presence of high gene flow – one of the most convincing reports of parapatric speciation in an aquatic organism from the Southern Hemisphere. In another study, we explored the role of adaptive diversification and recent sea-level changes as evolutionary drivers. That study pioneered phylogeographic reconstructions of radiations in South America (the coastal freshwater Odontesthes perugiae group), and also reported some of the most rapid speciation rates for a vertebrate (see publications below). Team members and collaborators: L Beheregaray, P Sunnucks (Monash), A Gosztonyi (Centro Nacional Patagónico, Argentina).

– Comparative Phylogeography and Speciation of Amazonian Fishes
In 2002 we implemented a research program on evolution of fishes in Amazonia, the basin home to the world’s richest freshwater fish fauna. This ambitious program started as a collaboration with Universidade do Amazonas (Brazil) and Yale University (USA), and was later funded by the ARC (DP0556496, Beheregaray 2005-2007). It aims to clarify the relative roles of natural selection and drift in population adaptation, divergence and speciation in the complex and understudied Amazonian fish fauna. So far, we have conducted nine field-expeditions in Amazonia that together covered over 6,000 Km of waterways and collected >4,000 samples from co-distributed fish species. We have produced several papers that pioneered the combination of genome scans with large-scale population genetics and phylogeographic datasets to understand evolution in Amazonia. Our findings indicate adaptive divergence and ecological speciation due to hydrochemical differences between major Amazonian rivers (i.e. differences in water colour and pH). In the Rio Negro basin, we have reported multiple cases of ancient cryptic species in lowland flooded-forest fish that likely evolved in response to Andean tectonic history. Team members and collaborators: L Beheregaray, G Cooke, M Sistrom, M Piggott and S Corrigan (Macquarie), N Chao (UFAM, Brazil), G Caccone (Yale).

– Comparative Phylogeography and Ecological Speciation of Elasmobranchs from the Gulf of California
The Gulf of California (GC) shows high ecological diversity, complex oceanography and active geological history, characteristics that make it suitable to study ecological speciation. This work aims to elucidate ecological and biogeographic factors that have shaped genetic structure and speciation in co-distributed elasmobranchs from the Gulf of California (GC) and the Pacific coast of Baja California Peninsula, in Mexico.  Study groups include sharks and rays from the genera RhinobatosSquatinaMustelus and Rhizoprionodon. Our results suggest previously unsuspected cryptic species that have probably diverged ecologically and also distinct populations that should be managed separately. These findings provide urgently needed information for conservation management of the heavily exploited elasmobranch fisheries in the region. This work represents the first comparative genetic analysis in elasmobranchs from the iconic GC ecosystem and has important implications for the study of the Gulf’s biodiversity and its origin and for improving our understanding about speciation in the sea. Team members and collaborators: J Sandoval-Castillo and L Beheregaray (Flinders), Oscar Sosa-Nishizaki (Center of Scientific Research of Ensenada, Mexico).

– Comparative Phylogeography and Phylogenetics of Australian Wobbegong Sharks
Wobbegongs sharks (Orectolobidae) are endemic to the temperate and tropical waters of the western Pacific and eastern Indian oceans, but are most diverse in Australian waters. We have proposed hypotheses about speciation and the biogeographic history of this family and provided evidence for recent events of diversification in this shark group. We have also reported on genetic evidence for a new species of wobbegong and are exploring phylogeographic history in co-distributed wobeggong sharks from the east coast of Australia. Team members and collaborators: S Corrigan (Macquarie), L Beheregaray, C Huveneers (Flinders).

– Phylogeography of perches and basses
This project aims to elucidate historical and current population genetic structure in golden perch, Macquarie perch, Australian bass, and estuary perch. We have reported on the influence of past climate and coastal oceanography in generating phylogeographic divergence and provided key information for conservation management of these recreationally important species. Team members and collaborators: L Beheregaray (Flinders), L Faulks, K Shaddick, T Schwartz (Macquarie), D Jerry (James Cook University), C Burridge (UTAS), W Fulton (DPI Fisheries VIC).

Select Publications

– Beheregaray LB, Levy JA (2000) Population genetics of the silverside Odontesthes argentinensis: evidence for speciation in an estuary of southern Brazil. Copeia 2000, 441-447.

– Beheregaray LB, Sunnucks P (2001) Fine-scale genetic structure, estuarine colonization and incipient speciation in the marine silverside fish Odontesthes argentinensisMolecular Ecology 10, 2849-2866.

– Beheregaray LB, Sunnucks P, Briscoe DA (2002) A rapid fish radiation associated with the last sea level changes in southern Brazil: the silverside Odontesthes perugiae complex. Proceedings of the Royal Society of London B 269, 65-73.

– Beheregaray LB, Caccone A (2007) Cryptic biodiversity in a changing world. Journal of Biology 6, 1-5.

– Cooke GM, Beheregaray LB (2007) Extremely high variability in the S72 intron of the Amazonian cardinal tetra (Paracheirodon axelrodi). Journal of Fish Biology 71, 132-140.

– Beheregaray LB (2008) Twenty years of Phylogeography: the state of the field and the challenges for the Southern Hemisphere. Molecular Ecology 17, 3754-3774.

– Corrigan S, Huveneers C, Schwartz TS, Harcourt RG, Beheregaray LB (2008) Genetic and reproductive evidence for two species of ornate wobbegong shark Orectolobus spp. on the Australian east coast. Journal of Fish Biology 73, 1662-1675.

– Faulks L, Gilligan D, Beheregaray LB (2008) Phylogeography of a threatened freshwater fish (Mogurnda adspersa) in eastern Australia: conservation implications. Marine and Freshwater Research 59, 89-96.

– Garrick RC, Dyer, RJ, Beheregaray LB, Sunnucks P (2008) Babies and bathwater: A comment on the premature obituary for nested clade phylogeographic analysis. Molecular Ecology 17, 1401-1403.

– Cooke GM, Chao NL & Beheregaray LB (2009) Phylogeography of a flooded forest specialist fish from central Amazonia based on intron DNA: the cardinal tetra Paracheirodon axelrodiFreshwater Biology 54, 1216-1232.

– Corrigan S, Beheregaray LB (2009) A recent shark radiation: molecular phylogeny, biogeography and speciation of wobbegong sharks (Orectolobidae). Molecular Phylogenetics and Evolution 52, 205-216.

– Sistrom MJ, Chao NL, Beheregaray LB (2009) Population history of the Amazonian one-lined pencilfish based on intron DNA data.  Journal of Zoology 278, 287–298.

– Teske PR, Beheregaray LB (2009) Evolution of seahorses’ upright posture was linked to Oligocene seagrass expansion. Biology Letters 5, 521-523.

– Faulks LK, Gilligan DM, Beheregaray LB (2010) Clarifying an ambiguous evolutionary history: range-wide phylogeography of an Australian freshwater fish, Golden Perch (Macquaria ambigua). Journal of Biogeography 37, 1329–1340.

– Faulks LK, Gilligan DM, Beheregaray LB (2010) Evolution and maintenance of divergent lineages in an endangered freshwater fish, Macquaria australasicaConservation Genetics 11, 921–934.

– Piggott M, Chao NL, Beheregaray LB (2011) Three fishes in one: cryptic species in an Amazonian floodplain forest specialist. Biological Journal of the Linnean Society 102, 391–403.

– Shaddick K, Burridge CP, Jerry DR, Gilligan DM, Truong K, Beheregaray LB (2011) Historical divergence with recent connectivity in a catadromous fish, the estuary perch (Macquaria colonorum). Canadian Journal of Fisheries and Aquatic Sciences 68, 304-318.

– Cooke G, Chao NL, Beheregaray LB (2012) Biogeographic history of the croaker genus Plagioscion (Sciaenidae): marine incursions, cryptic species and ecological diversification in Amazonia. Journal of Biogeography 39, 724–738.

– Cooke GM, Chao NL, Beheregaray LB (2012) Divergent natural selection with gene flow along major environmental gradients in Amazonia: Insights from genome scans, population genetics and phylogeography of the characin fish Triportheus albusMolecular Ecology doi: 10.1111/j.1365-294X.2012.05540.x.

– Cooke GM, Chao NL, Beheregaray LB (2012) Natural selection in the water: freshwater invasion and adaptation by water colour in the Amazonian pufferfish. Journal of Evolutionary Biology doi: 10.1111/j.1420-9101.2012.02514.x.

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