Rose L. Andrew

The detoxification limitation hypothesis : Where did it come from and where is it going?

The detoxification limitation hypothesis is firmly entrenched in the literature to explain various aspects of the interaction between herbivores and plant toxins. These include explanations for the existence of specialist and generalist herbivores and for the prevalence of each of these. The hypothesis suggests that the ability of mammalian herbivores to eliminate plant secondary metabolites (PSMs) largely determines which plants, and how much, they can eat. The value of the hypothesis is that it provides a clear framework for understanding how plant toxins might limit diet breadth. Thus, it is surprising, given its popularity, that there are few studies that provide experimental support either for or against the detoxification limitation hypothesis. There are two likely reasons for this. First, Freeland and Janzen did not formally propose the hypothesis, although it is implicit in their paper. Second, it is a difficult hypothesis to test, requiring an understanding of the metabolic pathways that lead to toxin elimination. Recent attempts to test the hypothesis appear promising. Results suggest that herbivores can recognize mounting saturation of a detoxification pathway and adjust their feeding accordingly to avoid intoxication. One strategy they use is to ingest a food containing a toxin that is metabolized by a different pathway. This demonstrates that careful selection of food plants is a key to existing in a chemically complex environment. As more studies characterize the detoxification products of PSMs, we will better understand how widespread this phenomenon is.

Marker-Based Quantitative Genetics in the Wild?: The Heritability and Genetic Correlation of Chemical Defenses in Eucalyptus

Marker-based methods for estimating heritability and genetic correlation in the wild have attracted interest because traditional methods may be impractical or introduce bias via G × E effects, mating system variation, and sampling effects. However, they have not been widely used, especially in plants. A regression-based approach, which uses a continuous measure of genetic relatedness, promises to be particularly appropriate for use in plants with mixed-mating systems and overlapping generations. Using this method, we found significant narrow-sense heritability of foliar defense chemicals in a natural population of Eucalyptus melliodora. We also demonstrated a genetic basis for the phenotypic correlation underlying an ecological example of conditioned flavor aversion involving different biosynthetic pathways. Our results revealed that heritability estimates depend on the spatial scale of the analysis in a way that offers insight into the distribution of genetic and environmental variance. This study is the first to successfully use a marker-based method to measure quantitative genetic parameters in a tree. We suggest that this method will prove to be a useful tool in other studies and offer some recommendations for future applications of the method.

Heritable variation in the foliar secondary metabolite sideroxylonal in Eucalyptus confers cross-resistance to herbivores

Plants encounter a broad range of natural enemies and defend themselves in diverse ways. The cost of defense can be reduced if a plant secondary metabolite confers resistance to multiple herbivores. However, there are few examples of positively correlated defenses in plants against herbivores of different types. We present evidence that a genetically variable chemical trait that acts as a strong antifeedant to mammalian herbivores of Eucalyptus also deters insect herbivores, suggesting a possible mechanism for cross-resistance. We provide field confirmation that sideroxylonal, an important antifeedant for mammalian herbivores, also determines patterns of damage by Christmas beetles, a specialist insect herbivore of Eucalyptus. In a genetic progeny trial of Eucalyptus tricarpa, we found significant heritabilities of sideroxylonal concentration (0.60), overall insect damage (0.34), and growth traits (0.30–0.53). Population of origin also had a strong effect on each trait. Negative phenotypic correlations were observed between sideroxylonal and damage, and between damage and growth. No relationship was observed between sideroxylonal concentration and any growth trait. Our results suggest that potential for evolution by natural selection of sideroxylonal concentrations is not strongly constrained by growth costs and that both growth and defense traits can be successfully incorporated into breeding programs for plantation trees.

Genomic variation across landscapes: insights and applications

The distribution of genomic variation across landscapes can provide insights into the complex interactions between the environment and the genome that influence the distribution of species, and mediate phenotypic adaptation to local conditions. High throughput sequencing technologies now offer unprecedented power to explore these interactions, allowing powerful inferences about historical processes of colonization, gene flow and divergence, as well as the identification of loci that mediate local adaptation. These landscape genomic approaches have been validated in model species and are now being applied to nonmodel organisms, including foundation species that have substantial effects on ecosystem processes. Here we review the growing field of landscape genomics from a very broad perspective. In particular, we describe the inferential power that is gained by taking a genome-wide view of genetic variation, strategies for study design to best capture adaptive variation, and how to apply this information to practical challenges, such as restoration.

SPATIAL DISTRIBUTION OF DEFENSE CHEMICALS AND MARKERS AND THE MAINTENANCE OF CHEMICAL VARIATION

Exploring the spatial distribution of variation in plant secondary metabolites is critical for understanding the evolutionary ecology of biochemical diversity in wild organisms. In the present study, concentrations of foliar sideroxylonal, an important and highly heritable defense chemical of Eucalyptus melliodora, displayed strong, fine-scale spatial autocorrelation. The spatial patterns observed could promote associational effects on herbivore foraging decisions, which may influence the selection pressures exerted on sideroxylonal content. Multiple chemical traits have roles in certain eucalypt-herbivore interactions, and the spatial characteristics of the herbivore foraging environment are therefore determined by these different factors. We used a model of E. melliodora intake by common brushtail possums (Trichosurus vulpecula), based on the combined effects of two chemical traits, to explore this idea and found that the spatial patterns were different to those of sideroxylonal alone. Spatial genetic autocorrelation, examined using microsatellites, was strong and occurred at a fine scale, implying that restricted gene flow might allow genetic patches to respond to selection relatively independently. Local two-dimensional genetic autocorrelation, explored using a new heuristic method, was highly congruent with the pattern of local phenotypic variation observed for sideroxylonal, suggesting that the genetic variance underlying the sideroxylonal variation is similarly structured. Our results suggest that the spatial distribution of genetic and phenotypic variation could influence both the selective pressure imposed by herbivores on eucalypt defenses and the potential of populations to respond to natural selection. Spatial context should be considered in future studies of plant-herbivore interactions.

Genetic and environmental contributions to variation and population divergence in a broad-spectrum foliar defence of Eucalyptus tricarpa

BACKGROUND AND AIMSnBoth environmental and genetic effects contribute to phenotypic variation within and among populations. Genetic differentiation of quantitative traits among populations has been shown in many species, yet it can also be accompanied by other genetic changes, such as divergence in phenotypic plasticity and in genetic variance. Sideroxylonal (a formylated phloroglucinol compound or FPC) is an important chemical defence in eucalypts. The effect of environmental variation on its production is a critical gap in our understanding of its genetics and evolution.nnnMETHODSnThe stability of genetic variation in sideroxylonal was assessed within and among populations of Eucalyptus tricarpa in three replicated provenance/progeny trials. The covariance structure of the data was also modelled to test whether genetic variances were consistent among populations and Fains test was applied for major gene effects.nnnKEY RESULTSnA significant genotype x environment interaction occurred at the level of population, and was related to temperature range and seasonality in source populations. Within-population genetic variation was not affected by genotype x environment effects or different sampling years. However, within-population genetic variance for sideroxylonal concentration differed significantly among source populations. Regression of family variance on family mean suggested that this trait is subject to major gene effects, which could explain the observed differences in genetic variances among populations.nnnCONCLUSIONSnThese results highlight the importance of replicated common-garden experiments for understanding the genetic basis of population differences. Genotype x environment interactions are unlikely to impede evolution or responses to artificial selection on sideroxylonal, but the lack of genetic variation in some populations may be a constraint. The results are broadly consistent with localized selection on foliar defence and illustrate that differentiation in population means, whether due to selection or to drift, can be accompanied by changes in other characteristics, such as plasticity and genetic variance.

Genetic, cytogenetic and morphological patterns in a mixed mulga population: evidence for apomixis

The mulga complex (Acacia aneura and closely related taxa) is a widespread group that is dominant in much of arid Australia. The group is taxonomically difficult, due to a complex interaction of sympatry and putative hybridisation between the major species, geographic variation within species and sympatric variation within A. aneura. Mulga is highly variable in a wide range of vegetative and reproductive characters and it is not unusual to find five or six distinct forms growing side by side. The aim of this project was to gain a better understanding of the relationships among mulga species and A. aneura varieties, as well as the maintenance of this variation. A single site in the Northern Territory, containing A. ayersiana, A. minyura and two varieties of A. aneura, was sampled intensively. Six morphotypes were observed in the field and five were strongly supported by morphometric analysis. Although the mulga complex is generally tetraploid (2n = 52), triploid (2n = 39) and pentaploid (2n = 65) seedlings were produced in the study population. Microsatellite primers developed for A. mangium (sect. Juliflorae) were amplified in individuals of each morphotype, resulting in genetic marker patterns consistent with polyploidy. Genetic and morphometric distances were correlated and differences between morphotypes account for 63% of the total genetic variation (φPT = 0.63, P < 0.001). Allele sequences confirmed the presence of genuine heterozygosity and clonality was suggested by the low genotypic diversity and the lack of allele segregation. Seedlings had identical genotypes to the maternal plants and polyembryony was observed in each taxon, consistent with apomictic reproduction. Both apomixis and ploidy level variation may restrict gene flow among morphotypes, playing a role in the maintenance of morphological diversity at the study site. The success of the group in arid and semi-arid Australia may also be due, in part, to these factors. SB enet or v ul R. L.

Molecular phylogenetics of the Australian acacias of subg. Phyllodineae (Fabaceae: Mimosoideae) based on the trnK intron

With over 960 species, Acacia is the largest genus of plants in Australia with all but nine of these species classified as subgenus Phyllodineae. DNA sequences for the chloroplast trnK region were sequenced for over 100 species to test sectional classification and survey species relationships within this subgenus. Only one of the seven recognised sections was found to be monophyletic; however, the close relationship of sect. Botrycephalae to certain racemose, uninerved species of sect. Phyllodineae is confirmed. Support is found for an expanded version of Vassals Pulchelloidea, with the addition of sect. Lycopodiifoliae and several members of sect. Phyllodineae. These species, while morphologically distinct in adult foliage, possess similar seedling characteristics. The multinerved species are unresolved, indicating a rapid morphological radiation with little chloroplast sequence divergence among these species. The low levels of sequence divergence, large numbers of morphological species groups and the adaptive radiation of the group are discussed.

Intensive sampling identifies previously unknown chemotypes, population divergence and biosynthetic connections among terpenoids in Eucalyptus tricarpa

Australian members of the Myrtaceae produce large quantities of ecologically and economically important terpenes and display abundant diversity in both yield and composition of their oils. In a survey of the concentrations of leaf terpenes in Eucalyptus tricarpa (L.A.S. Johnson) L.A.S. Johnson & K.D. Hill, which were previously known from few samples, exceptional variability was found in composition. The aim was to characterize the patterns of variation and covariation among terpene components in this species and to use this information to enhance our understanding of their biosynthesis. There were marked discontinuities in the distributions of numerous compounds, including the overall proportions of mono- and sesquiterpenes, leading us to delineate three distinct chemotypes. Overall, positive covariation predominated, but negative covariation suggested competitive interactions involved in monoterpene synthesis. Two groups of covarying monoterpenes were found, each of which was positively correlated with a group of sesquiterpenes and negatively correlated with the alternate sesquiterpene group. These results imply substantial cross-talk between mono- and sesquiterpene biosynthesis pathways. However, only those compounds hypothesized to share final carbocation intermediates or post-processing steps were strongly positively correlated within chemotypes. This suggests that the broader patterns of covariation among groups of compounds may result from co-regulation of multiple biosynthetic genes, controlling the complex terpene profiles of the chemotypes of Eucalyptus.