Matthew J. Christmas

Constraints to and conservation implications for climate change adaptation in plants

Contemporary climate change is having widespread impacts on plant populations. Understanding how plants respond to this change is essential to our efforts to conserve them. The key climate responses of plant populations can be categorised into one of three types: migration, in situ adaptation, or extirpation. If populations are to avoid extirpation then migration and/or in situ adaptation is essential. In this review we first articulate the current and future constraints of plant populations, but trees in particular, to the different adaptation strategies (e.g. space availability, rate of change, habitat fragmentation, niche availability). Secondly, we assess the use of the most appropriate methods (e.g. natural environmental gradients, genome and transcriptome scans) for assessing and understanding adaptive responses and the capacity to adapt to future challenges. Thirdly, we discuss the best conservation approaches (e.g. assisted migration, biodiversity corridors, ex situ strategies) to help overcome adaptive constraints in plants. Our synthesis of plant, and particularly tree, responses and constraints to climate change adaptation, combined with the identification of conservation strategies designed to overcome constraints, will help deliver effective management actions to assist adaptation in the face of current and future climate change.

Higher Levels of Multiple Paternities Increase Seedling Survival in the Long-Lived Tree Eucalyptus gracilis

Studying associations between mating system parameters and fitness in natural populations of trees advances our understanding of how local environments affect seed quality, and thereby helps to predict when inbreeding or multiple paternities should impact on fitness. Indeed, for species that demonstrate inbreeding avoidance, multiple paternities (i.e. the number of male parents per half-sib family) should still vary and regulate fitness more than inbreeding – named here as the ‘constrained inbreeding hypothesis’. We test this hypothesis in Eucalyptus gracilis, a predominantly insect-pollinated tree. Fifty-eight open-pollinated progeny arrays were collected from trees in three populations. Progeny were planted in a reciprocal transplant trial. Fitness was measured by family establishment rates. We genotyped all trees and their progeny at eight microsatellite loci. Planting site had a strong effect on fitness, but seed provenance and seed provenance × planting site did not. Populations had comparable mating system parameters and were generally outcrossed, experienced low biparental inbreeding and high levels of multiple paternity. As predicted, seed families that had more multiple paternities also had higher fitness, and no fitness-inbreeding correlations were detected. Demonstrating that fitness was most affected by multiple paternities rather than inbreeding, we provide evidence supporting the constrained inbreeding hypothesis; i.e. that multiple paternity may impact on fitness over and above that of inbreeding, particularly for preferentially outcrossing trees at life stages beyond seed development.

Finding needles in a genomic haystack: targeted capture identifies clear signatures of selection in a nonmodel plant species.

Teasing apart neutral and adaptive genomic processes and identifying loci that are targets of selection can be difficult, particularly for nonmodel species that lack a reference genome. However, identifying such loci and the factors driving selection have the potential to greatly assist conservation and restoration practices, especially for the management of species in the face of contemporary and future climate change. Here, we focus on assessing adaptive genomic variation within a nonmodel plant species, the narrow‐leaf hopbush (Dodonaea viscosa ssp. angustissima), commonly used for restoration in Australia. We used a hybrid‐capture target enrichment approach to selectively sequence 970 genes across 17 populations along a latitudinal gradient from 30°S to 36°S. We analysed 8462 single‐nucleotide polymorphisms (SNPs) for FST outliers as well as associations with environmental variables. Using three different methods, we found 55 SNPs with significant correlations to temperature and water availability, and 38 SNPs to elevation. Genes containing SNPs identified as under environmental selection were diverse, including aquaporin and abscisic acid genes, as well as genes with ontologies relating to responses to environmental stressors such as water deprivation and salt stress. Redundancy analysis demonstrated that only a small proportion of the total genetic variance was explained by environmental variables. We demonstrate that selection has led to clines in allele frequencies in a number of functional genes, including those linked to leaf shape and stomatal variation, which have been previously observed to vary along the sampled environmental cline. Using our approach, gene regions subject to environmental selection can be readily identified for nonmodel organisms.

Individual and collective choice: parallel prospecting and mining in ants

Decision making is of crucial importance in the lives of both animals and humans. How decisions of group members scale up to group decisions is of great interest. Accordingly, we gave homeless ant colonies (n = 67) in three experiments a choice between two nest sites (with small, big or mixed sand grains), each of which had to be excavated to be habitable. Among the colonies that chose only one of the new nest sites, all preferred the ones that could be excavated most easily and quickly. There are interesting parallels between the collective choice of mining sites and the ability of certain ants to select short cuts; both involve positive feedback. However, in this paper, we discuss a mechanism whereby collective co-ordination in the production of social infrastructure can occur in the absence of signalling.

Targeted capture to assess neutral genomic variation in the narrow-leaf hopbush across a continental biodiversity refugium

The Adelaide geosyncline, a mountainous region in central southern Australia, is purported to be an important continental refugium for Mediterranean and semi-arid Australian biota, yet few population genetic studies have been conducted to test this theory. Here, we focus on a plant species distributed widely throughout the region, the narrow-leaf hopbush, Dodonaea viscosa ssp. angustissima, and examine its genetic diversity and population structure. We used a hybrid-capture target enrichment technique to selectively sequence over 700 genes from 89 individuals across 17 sampling locations. We compared 815 single nucleotide polymorphisms among individuals and populations to investigate population genetic structure. Three distinct genetic clusters were identified; a Flinders/Gammon ranges cluster, an Eastern cluster, and a Kangaroo Island cluster. Higher genetic diversity was identified in the Flinders/Gammon Ranges cluster, indicating that this area is likely to have acted as a refugium during past climate oscillations. We discuss these findings and consider the historical range dynamics of these populations. We also provide methodological considerations for population genomics studies that aim to use novel genomic approaches (such as target capture methods) on non-model systems. The application of our findings to restoration of this species across the region are also considered.

Bioclimatic transect networks: powerful observatories of ecological change

Abstract Transects that traverse substantial climate gradients are important tools for climate change research and allow questions on the extent to which phenotypic variation associates with climate, the link between climate and species distributions, and variation in sensitivity to climate change among biomes to be addressed. However, the potential limitations of individual transect studies have recently been highlighted. Here, we argue that replicating and networking transects, along with the introduction of experimental treatments, addresses these concerns. Transect networks provide cost‐effective and robust insights into ecological and evolutionary adaptation and improve forecasting of ecosystem change. We draw on the experience and research facilitated by the Australian Transect Network to demonstrate our case, with examples, to clarify how population‐ and community‐level studies can be integrated with observations from multiple transects, manipulative experiments, genomics, and ecological modeling to gain novel insights into how species and systems respond to climate change. This integration can provide a spatiotemporal understanding of past and future climate‐induced changes, which will inform effective management actions for promoting biodiversity resilience.

Transcriptome sequencing, annotation and polymorphism detection in the hop bush, Dodonaea viscosa

BackgroundThe hop bush, Dodonaea viscosa, is a trans-oceanic species distributed oversix continents. It evolved in Australia where it is found over a wide range of habitat types and is an ecologically important species. Limited genomic resources are currently available for this species, thus our understanding of its evolutionary history and ecological adaptation is restricted. Here, we present a comprehensive transcriptome dataset for future genomic studies into this species.MethodsWe performed Illumina sequencing of cDNA prepared from leaf tissue collected from seven populations of D. viscosa ssp. angustissima and spatulata distributed along an environmental gradient in South Australia. Sequenced reads were assembled to provide a transcriptome resource. Contiguous sequences (contigs) were annotated using BLAST searches against the NCBI non-redundant database and gene ontology definitions were assigned. Single nucleotide polymorphisms were detected for the establishment of a genetic marker set. A comparison between the two subspecies was also carried out.ResultsIllumina sequencing returned 268,672,818 sequence reads, which were de novoassembled into 105,125 contigs. Contigs with significant BLAST alignments (E value < 1e-5)numbered at 44,191, with 38,311 of these having their most significant hits to sequences from land plant species. Gene Ontology terms were assigned to 28,440 contigs and KEGG analysis identified 146 pathways that the gene products from 5,070 contigs are potentially involved in. The subspecies comparison identified 8,494 fixed SNP differences across 3,979 contiguous sequences, indicating a level of genetic differentiation between them. Across all samples, 248,235 SNPs were detected.ConclusionsWe have established a significant genomic data resource for D. viscosa,providing a comprehensive transcriptomic reference. Genetic differences among morphologically distinct subspecies were found. A wide range of putative gene regions were identified along with a large set of variable SNP markers, providing a basis for studies into the evolution and ecological adaptation of D. viscosa.