Phylogeography and population genetics of Australian freshwater rainbowfishes

Abstract

Diversity in Australia’s freshwater fish fauna is relatively depauperate when compared toother landmasses. However the family Melanotaeniidae is one of Australia’s most widespread andspeciose groups of freshwater fishes. As such, they are an ideal group in which to examinefreshwater phylogeography within Australia, as they offer the opportunity to compare species withdifferent niches, but similar evolutionary history. This dissertation investigates patterns of geneticdiversity in three species of Australian freshwater rainbowfishes, two co-distributed species withdistinct niches in undisturbed habitat, and one species in an urban habitat, and explores thehistorical and contemporary processes that have influenced them.In my first chapter I used two co-distributed Melanotaenia species to test the hypothesis thata widespread habitat generalist will have lower levels of genetic diversity and population structurethan a closely related habitat specialist. I used sequence from one mitochondrial gene and onenuclear gene to investigate patterns of genetic diversity in M. splendida and M. trifasciata and todetermine how differences in habitat preference and historical changes in drainage boundaries haveaffected patterns of connectivity and isolation. M. splendida, a widespread species found in the vastmajority of freshwater habitats in northern Australia, showed high levels of genetic diversity, andvery little population structure across its range. Conversely, M. trifasciata, having a greatlycontracted distribution to the northernmost rivers of Queensland and the Northern Territory andhabitat preference for faster flowing, highly oxygenated upland streams, showed extremely highlevels of population structure. While phylogeographic patterns differed, both showed a strongrelationship between stream length and genetic distance. For M. trifasciata genetic distance wasbest explained by stream length within catchments, and an ocean distance at 100x coast length,likely reflecting infrequent dispersal between catchments at times of low sea level (r2 = 0.82). M.splendida had a much shallower relationship with geographic distance, and genetic distance wasbest explained by stream length and a weaker ocean distance (10x coast length), suggesting greaterrates of gene exchange. These results suggest that, although these species are co-distributed theyappear to have experienced different evolutionary histories, with differences in habitat preferencewithin waterways resulting in contrasting scales of genetic patterns.In chapter two I identified hybrid zones between co-distributed M. splendida and M.trifasciata at the periphery of M. trifasciata's distribution. I used morphological identification,mtDNA sequences and two nuclear single nucleotide polymorphism (SNP) diagnostic restrictionassays to characterize incidence, levels and directionality of gene flow between these tworeciprocally monophyletic taxa. Four populations were identified as having undergone extensivehybridization between M. splendida and M. trifasciata. Patterns of gene flow between the two taxawere different in different hybridizing populations with complete mitochondrial capture evident in two populations, uni-directional introgression in a third population, and a complete mixture ofmorphological hybrids and bi-directional gene exchange in the fourth population. This diversity inpatterns of hybridization between two species is unusual and could potentially be due to localenvironmental conditions, although further research is required to determine the processes that aredriving this pattern.In chapter four I investigated how different aspects of habitat degradation affect the geneticdiversity of an Australian native rainbowfish, Rhadinocentrus ornatus, distributed in a highlydeveloped region (southeast Queensland) and what impacts this may have on this species’conservation status. Based on mtDNA sequence data from 327 individuals and 20 populations, Iidentified three distinct genetic lineages that were allopatric at the stream level. Indicators of habitatdegradation had large negative effects on measures of genetic diversity, with close proximity tourban development and alterations to waterways associated with drastically reduced measures ofgenetic diversity across three distinct mtDNA lineages (evolutionary significant units). Loweffective population sizes and low standing genetic variation in degraded habitats may result inreduced adaptive potential in this already threatened narrow range endemic. The only surveyedpopulations with high genetic diversity were found in already protected national parks. Manyhistorical populations of R. ornatus in the highly developed Greater Brisbane Region are alreadyprobably extinct, and without further study and management this may be the fate of presentlygenetically depauperate populations in urban areas.This thesis represents the most comprehensive study to date of rainbowfish populationgenetics. Researching multiple species within the same genus, and sampling a large proportion ofeach species range has provided me with substantial power to infer the evolutionary andcontemporary processes that have shaped genetic diversity and connectivity in three species.Contrasting phylogeographic patterns from two co-distributed species with different environmentalniches occurring in relatively pristine habitats provided insight into long-term evolutionaryprocesses. Sampling large numbers of populations, both in pristine and developed habitats, providedinformation on ecologically relevant forces shaping fine scale connectivity. This work adds togrowing literature on population genetics of Australian freshwater fishes and specifically howhistorical changes in landscape connectivity, hybridization and urban development shape patterns ofgenetic diversity in Australian rainbowfishes.