Margaret Byrne

Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota

The integration of phylogenetics, phylogeography and palaeoenvironmental studies is providing major insights into the historical forces that have shaped the Earths biomes. Yet our present view is biased towards arctic and temperate/tropical forest regions, with very little focus on the extensive arid regions of the planet. The Australian arid zone is one of the largest desert landform systems in the world, with a unique, diverse and relatively well-studied biota. With foci on palaeoenvironmental and molecular data, we here review what is known about the assembly and maintenance of this biome in the context of its physical history, and in comparison with other mesic biomes. Aridification of Australia began in the Mid-Miocene, around 15 million years, but fully arid landforms in central Australia appeared much later, around 1-4 million years. Dated molecular phylogenies of diverse taxa show the deepest divergences of arid-adapted taxa from the Mid-Miocene, consistent with the onset of desiccation. There is evidence of arid-adapted taxa evolving from mesic-adapted ancestors, and also of speciation within the arid zone. There is no evidence for an increase in speciation rate during the Pleistocene, and most arid-zone species lineages date to the Pliocene or earlier. The last 0.8 million years have seen major fluctuations of the arid zone, with large areas covered by mobile sand dunes during glacial maxima. Some large, vagile taxa show patterns of recent expansion and migration throughout the arid zone, in parallel with the ice sheet-imposed range shifts in Northern Hemisphere taxa. Yet other taxa show high lineage diversity and strong phylogeographical structure, indicating persistence in multiple localised refugia over several glacial maxima. Similar to the Northern Hemisphere, Pleistocene range shifts have produced suture zones, creating the opportunity for diversification and speciation through hybridisation, polyploidy and parthenogenesis. This review highlights the opportunities that development of arid conditions provides for rapid and diverse evolutionary radiations, and re-enforces the emerging view that Pleistocene environmental change can have diverse impacts on genetic structure and diversity in different biomes. There is a clear need for more detailed and targeted phylogeographical studies of Australias arid biota and we suggest a framework and a set of a priori hypotheses by which to proceed.

Assessing the benefits and risks of translocations in changing environments: a genetic perspective

Translocations are being increasingly proposed as a way of conserving biodiversity, particularly in the management of threatened and keystone species, with the aims of maintaining biodiversity and ecosystem function under the combined pressures of habitat fragmentation and climate change. Evolutionary genetic considerations should be an important part of translocation strategies, but there is often confusion about concepts and goals. Here, we provide a classification of translocations based on specific genetic goals for both threatened species and ecological restoration, separating targets based on ‘genetic rescue’ of current population fitness from those focused on maintaining adaptive potential. We then provide a framework for assessing the genetic benefits and risks associated with translocations and provide guidelines for managers focused on conserving biodiversity and evolutionary processes. Case studies are developed to illustrate the framework.

The genome of Eucalyptus grandis

Eucalypts are the world’s most widely planted hardwood trees. Their outstanding diversity, adaptability and growth have made them a global renewable resource of fibre and energy. We sequenced and assembled >94% of the 640-megabase genome of Eucalyptus grandis. Of 36,376 predicted protein-coding genes, 34% occur in tandem duplications, the largest proportion thus far in plant genomes. Eucalyptus also shows the highest diversity of genes for specialized metabolites such as terpenes that act as chemical defence and provide unique pharmaceutical oils. Genome sequencing of the E. grandis sister species E. globulus and a set of inbred E. grandis tree genomes reveals dynamic genome evolution and hotspots of inbreeding depression. The E. grandis genome is the first reference for the eudicot order Myrtales and is placed here sister to the eurosids. This resource expands our understanding of the unique biology of large woody perennials and provides a powerful tool to accelerate comparative biology, breeding and biotechnology.

An integrated genetic linkage map for eucalypts using RFLP, RAPD and isozyme markers

An integrated genetic linkage map for E. nitens was constructed in an outbred three-generation pedigree. Analysis of 210 RFLP, 125 RAPD and 4 isozyme loci resulted in 330 markers linked in 12 linkage groups covering 1462 cM (n=11 in eucalypts). The 12th linkage group is comprised of only 5 markers and will probably coalesce with another linkage group when further linked loci are located. Co-dominant RFLP loci segregating in both parents were used to integrate linkages identified in the male and female parents. Differences in recombination frequencies in the two parents were observed for a number of pairs of loci, and duplication of sequences was identified both within and between linkage groups. The markers were distributed randomly across the genome except for the RFLPs in linkage group 10 and for some loci showing segregation distortion, which were clustered into three regions of the map. The use of a large number of co-dominant RFLP loci in this map enables it to be used in other pedigrees of E. nitens and forms a basis for the detection and location of QTL in E. nitens and other eucalypt species.

Population divergence in the chloroplast genome of Eucalyptus nitens

Variation in the chloroplast genome of Eucalyptus nitens was assessed for ten individuals from each of eight populations covering the natural range of the species. Twenty-five mutations were detected which were distributed over 13 haplotypes. The mutations were present both within and between populations. The level of nucleotide diversity within the species was high and the majority of the variation was distributed between populations and regions. The level and distribution of haplotype diversity were similar to those of the nucleotide diversity. The interpopulational variation may be related to the large range and disjunct populations that characterize the species, due to the effects of isolation and genetic drift. There were three mutations which were unique and fixed in one small population. Individuals in the species could be distinguished into two cpDNA groups. The distribution of these groups was not consistent with any geographical pattern. The distribution of the cpDNA groups suggests that they are of ancient origin and predate the isolation of the regions. The pattern of cpDNA variation is not consistent with patterns of variation in morphological traits.

A genetic linkage map for Eucalyptus globulus with candidate loci for wood, fibre, and floral traits

Abstract A genetic linkage map containing potential candidate loci for wood, fibre and floral traits has been constructed for Eucalyptus globulus (Labill.) based on the segregation of 249 codominant loci in an outbred F1 population of 148 individuals. The map contains 204 RFLP loci, including 31 cambium-specific expressed sequence tags (ESTs) and 14 known function genes, and 40 microsatellite and five isozyme loci. Independent male and female maps were constructed, and the 98 loci (39%) that segregated in both parents were used to combine the parental maps into an integrated map. The 249 loci mapped to 11 major linkage groups (n=11 in eucalypts) and a 12th small linkage group containing three loci that segregated in the male parent only. Total map distance is 1375 cM with an average interval of 6 cM. Forty one of the mapped loci identify known proteins (five isozymes) or sequences with known function (14 genes and 22 ESTs). The mapped genes include enzymes involved in lignin and cell-wall polysaccharide biosynthesis, and floral-development genes. This map will be used to locate quantitative trait loci for wood, fibre, and other traits in Eucalyptus.

Biological invasions, climate change and genomics

The rate of biological invasions is expected to increase as the effects of climate change on biological communities become widespread. Climate change enhances habitat disturbance which facilitates the establishment of invasive species, which in turn provides opportunities for hybridization and introgression. These effects influence local biodiversity that can be tracked through genetic and genomic approaches. Metabarcoding and metagenomic approaches provide a way of monitoring some types of communities under climate change for the appearance of invasives. Introgression and hybridization can be followed by the analysis of entire genomes so that rapidly changing areas of the genome are identified and instances of genetic pollution monitored. Genomic markers enable accurate tracking of invasive species’ geographic origin well beyond what was previously possible. New genomic tools are promoting fresh insights into classic questions about invading organisms under climate change, such as the role of genetic variation, local adaptation and climate pre‐adaptation in successful invasions. These tools are providing managers with often more effective means to identify potential threats, improve surveillance and assess impacts on communities. We provide a framework for the application of genomic techniques within a management context and also indicate some important limitations in what can be achieved.

Identification and mode of action of quantitative trait loci affecting seedling height and leaf area in Eucalyptus nitens

Abstract Regions of the genome influencing height and leaf area in seedlings of a three-generation outbred pedigree of Eucalyptus nitens have been identified. Three QTLs affecting height and two QTLs affecting leaf area were located using single-factor analysis of variance. The three QTLs affecting height each explained between 10.3 and 14.7% of the phenotypic variance, while the two QTLs for leaf area each explained between 9.8 and 11.6% of the phenotypic variation. Analysis of fully informative marker loci linked to the QTLs enabled the mode of action of the QTLs to be investigated. For three loci the QTL effect segregated from only one parent, while for two loci the QTL showed multiple alleles and the effect segregated from both parents in the pedigree. The two QTLs affecting leaf area were located in the same regions as two of the QTLs affecting height. Analysis of these regions with fully informative markers showed that both QTLs were linked to the same markers, but one had a similar size of effects and a similar mode of action for both height and leaf area, whilst the other showed a different mode of action for the two traits. These regions may contain two closely linked genes or may involve a single gene with a pleiotrophic effect on both height and leaf area. The QTL with the greatest effect showed multiple alleles and an intra-locus interaction that reduced the size of the effect. Assessment for two of the QTLs in a second related family did not show an effect associated with the marker loci; however, this was consistent with the mode of action of these QTLs and the pattern of inheritance in the second family.

A framework for incorporating evolutionary genomics into biodiversity conservation and management

Evolutionary adaptation drives biodiversity. So far, however, evolutionary thinking has had limited impact on plans to counter the effects of climate change on biodiversity and associated ecosystem services. This is despite habitat fragmentation diminishing the ability of populations to mount evolutionary responses, via reductions in population size, reductions in gene flow and reductions in the heterogeneity of environments that populations occupy. Research on evolutionary adaptation to other challenges has benefitted enormously in recent years from genomic tools, but these have so far only been applied to the climate change issue in a piecemeal manner. Here, we explore how new genomic knowledge might be combined with evolutionary thinking in a decision framework aimed at reducing the long-term impacts of climate change on biodiversity and ecosystem services. This framework highlights the need to rethink local conservation and management efforts in biodiversity conservation. We take a dynamic view of biodiversity based on the recognition of continuously evolving lineages, and we highlight when and where new genomic approaches are justified. In general, and despite challenges in developing genomic tools for non-model organisms, genomics can help management decide when resources should be redirected to increasing gene flow and hybridisation across climate zones and facilitating in situ evolutionary change in large heterogeneous areas. It can also help inform when conservation priorities need to shift from maintaining genetically distinct populations and species to supporting processes of evolutionary change. We illustrate our argument with particular reference to Australia’s biodiversity.

Extensive pollen dispersal in a bird-pollinated shrub, Calothamnus quadrifidus, in a fragmented landscape

Pollen dispersal was investigated in six populations of Calothamnus quadrifidus, a bird‐pollinated shrub in the fragmented agricultural region of southern Western Australia. Paternity analysis using six microsatellite loci identified a pollen source within populations for 67% of seedlings, and the remainder were assumed to have arisen from pollen sources outside the populations. Outcrossing was variable, ranging from 5% to 82%, and long‐distance pollen dispersal was observed in all populations with up to 43% of pollen sourced from outside the populations over distances of up to 5 km. This extensive pollen immigration was positively associated with population size but not isolation. Comparison of two populations of similar size but different density showed greater internal pollination and less selfing in the denser population, suggesting an influence of density on pollinator behaviour. The study revealed extensive long‐distance pollen dispersal for C. quadrifidus within this fragmented agricultural landscape and highlighted the interaction between reserve populations and isolated road verge remnants in maintaining genetic connectivity at the landscape scale.