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Paratya Australiensis) A GENOMICS PERSPECTIVE OF SPECIES AND SPECIATION IN AN ATYID SHRIMP (PARATYA AUSTRALIENSIS) Kimberley Rogl BAppSc BSc (Hons) Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy School of Biology and Environmental Sciences Science and Engineering Faculty Queensland University of Technology 2020 Keywords Atyid, cryptic species, freshwater shrimp, hybridisation, next-generation sequencing, phylogenomics, reproductive isolation, SNP analysis, speciation, speciation genes, speciation genomics, species complex, transcriptomics, Paratya australiensis A GENOMICS PERSPECTIVE OF SPECIES AND SPECIATION IN AN ATYID SHRIMP (PARATYA AUSTRALIENSIS) i Abstract The speciation debate in evolutionary science is long and protracted, as evidenced by the multitude of concepts regarding species and speciation, but understanding the nature of species is of central importance in the study of biology and ecology. Traditional approaches for investigating speciation (eg. behavioural or morphological) have not always provided sufficient insight into understanding the processes involved. While modern molecular techniques provide different perspectives to help address these biological questions, it is often difficult to find natural populations outside the laboratory to recognise speciation in which to apply them. A human-induced translocation event in the 1990s of the atyid shrimp, Paratya australiensis, inadvertently brought together two very divergent lineages of the species, resulting in extreme non-random mating. While, the species status of P. australiensis has previously been debated, it is currently considered monotypic. Other research, however, suggests that this single species may indeed be a complex of cryptic species (up to nine species) or is at least in the final stages of speciating. Consequently, this system provides an excellent opportunity to investigate speciation from a genetics/genomics perspective. In the Brisbane River, SE Queensland in 1993, 10,000 shrimp from one lineage (Kilcoy Creek) were translocated to another site (Branch Creek) where a divergent lineage (~6% for mtDNA COI) existed. The majority of resulting F1 juveniles were hybrids resulting from Branch Creek males mating with Kilcoy Creek females (there were no hybrids found from the reverse cross). However, when the same site was sampled after these F1 reached adult stage some months later, the hybrids had significantly decline in number relative to the number of individuals from matings within lineages, indicating reduced fitness in these hybrids. The purpose of this study was to investigate the genetic architecture of individuals from both pure lineages and of individuals across the hybrid zone to gain insight into the process of speciation at the molecular level. First, a comparative transcriptomic approach was used on the two highly divergent lineages of P. australiensis to identify genes of interest that may be associated with adaptation to local environments that may contribute to the observed breakdown in mate recognition. Differential gene expression (DGE) analysis showed ii A GENOMICS PERSPECTIVE OF SPECIES AND SPECIATION IN AN ATYID SHRIMP (PARATYA AUSTRALIENSIS) 660 highly differentially expressed transcripts between the two populations (eg. genes associated with temperature tolerance, osmoregulation, egg size control and other life history characteristics). Hard variant calling revealed 2,554 filtered single nucleotide polymorphisms (SNPs); overall, this high number is consistent with neutral divergence shown in previous studies. However, SNPs at some of these genes indicated that local adaptation associated with energy production, temperature tolerance, etc. has significantly contributed to how these lineages have evolved and diverged while adapting to their respective habitats. The second research chapter incorporated the two pure lineages along with individuals from the known hybrid zone to identify genes directly involved in speciation or reproductive isolation. Using transcriptomics, five speciation genes identified in the literature (adenylate cyclase, arylsulfatase, heat shock 70, tcP-1, and triosephosphate isomerase) appeared to be under purifying selection. Multiple genes were identified through gene ontology that are involved in the reproductive process but a single gene (takeout protein – identified as part of the enzymatic pathway associated with courtship behaviour in Drosophila) showed a signature of positive selection. Furthermore, The DGE analysis revealed a cytonuclear interaction relating to temperature and oxygen transport that had not previously been seen in P. australiensis. This pattern fits the Dobzhansky-Muller model where speciation is underpinned by a few genes interacting between the mitochondrial and nuclear genomes. The third component of research was to investigate whether the asymmetrical hybridisation was still ongoing in the known hybrid zone in Branch Creek. Of particular interest was whether, after 25 generations of interbreeding (i.e. hybridisation, backcrossing etc.), the two lineages had become homogenised or if there were signatures of continued deviation from random mating seen in both mitochondrial and nuclear genomes. A SNP approach was used and after variant calling, 35,704 SNPs were found across the two pure lineages and the nine hybrid zone individuals. Multiple analyses (identity by state, principal component, and relatedness) of these SNPs showed that hybridisation is still ongoing as evidenced by the detection of early generation hybrids. While variation in nuclear genomes of the hybrid zone individuals suggested that hybridisation was still occurring, eight out of these nine individuals had the introduced mtDNA (i.e. from Kilcoy Creek), suggesting strong A GENOMICS PERSPECTIVE OF SPECIES AND SPECIATION IN AN ATYID SHRIMP (PARATYA AUSTRALIENSIS) iii selection was still present, even when large parts of their nuclear genomes had returned to a similar profile as an original Branch Creek resident. There is a strong indication that given sufficient time, the introduced mtDNA (either through purifying or sexual selection) may send the Branch Creek lineage extinct. Finally, the biogeographic history of the nine divergent P. australiensis lineages was investigated using the mitochondrial cytochrome oxidase I (COI) gene; previous problems with polytomies were resolved with whole mitogenome analysis of the two lineages used in this study. From this, the COI phylogeny can more confidently be relied upon to provide an accurate portrayal of the diversification/divergence history of the P. australiensis species complex. The phylogeny showed three distinct range expansions that have occurred in a south to north direction. It is interesting to note that after these range expansions, none of the currently known lineages have ever been found in sympatry. This suggests that when two lineages have come together in the past, non-random mating in every case has led to the fixation of one lineage and the extinction of the other. Overall, this project provides an extensive genomic resource to investigate the nature of species and speciation in P. australiensis. From the results, it can be inferred that P. australiensis sits along the speciation continuum, towards becoming a species complex (cryptic or not). There is evidence that a single lineage is dominant over others that it comes into contact with (i.e. through hybridisation, one lineage goes extinct - consistent with Paterson’s recognition species concept) before positive reinforcement can occur (sensu Dobzhansky/Mayr biological species concept). The cytonuclear incompatibilities are the perfect example of a few genes interacting that results in lower fitness in the hybrid offspring (i.e. genic species concept). iv A GENOMICS PERSPECTIVE OF SPECIES AND SPECIATION IN AN ATYID SHRIMP (PARATYA AUSTRALIENSIS) Table of Contents Keywords .................................................................................................................................. i Abstract .................................................................................................................................... ii List of Figures ........................................................................................................................ vii List of Tables .......................................................................................................................... ix List of Abbreviations ................................................................................................................ x Statement of Original Authorship ........................................................................................... xi Acknowledgements ................................................................................................................ xii Chapter 1: Introduction ...................................................................................... 1 1.1 Background ..................................................................................................................... 2 1.2 Aims of the current project ........................................................................................... 23 1.3 Thesis Outline ............................................................................................................... 24 Chapter 2: A transcriptome-wide assessment of differentially expressed genes among two highly divergent, yet sympatric, lineages of the freshwater atyid shrimp, Paratya australiensis
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