A geographic mosaic of genetic variation within a foundation tree species and its community-level consequences.

Knowledge of the manner in which genetic variation within a tree species affects associated communities and ecosystem processes across its entire range is important for understanding how geographic mosaics of genetic interactions might develop and support different communities. While numerous studies have investigated the community and ecosystem consequences of genetic variation at the hybrid cross type or genotype level within a species, none has investigated the community-level effects of intraspecific genetic variation across the geographic range of a widespread species. This is the scale at which geographic mosaics of coevolution are hypothesized to exist. Studies at this level are particularly important for foundation tree species, which typically support numerous microbial, fungal, plant, and animal communities. We studied genetic variation across eight geographical races of the forest tree Eucalyptus globulus representing its natural distribution across southeastern Australia. The study was conducted in a 15-year-old common garden trial based on families derived from single-tree open-pollinated seed collections from the wild. Neutral molecular genetic variation within E. globulus was also assessed and compared with genetic divergence in the phenotypic and community traits. Three major findings emerged. First, we found significant genetically based, hierarchical variation in associated communities corresponding to geographical races of E. globulus and families within races. Second, divergence in foliar communities at the racial level was associated with genetically based divergence in specific leaf morphological and chemical traits that have known defensive functions. Third, significant positive correlations between canopy community dissimilarity and both neutral molecular genetic and leaf quantitative genetic dissimilarity at the race level supported a genetic similarity rule. Our results argue that genetic variation within foundation tree species has the potential to be a significant driver of the geographical mosaics of variation typical of forest communities, which could have important ecological and evolutionary implications.

Biodiversity consequences of genetic variation in bark characteristics within a foundation tree species.

The developing field of community genetics has the potential to broaden the contribution of genetics to conservation biology by demonstrating that genetic variation within foundation plant species can act to structure associated communities of microorganisms, invertebrates, and vertebrates. We assessed the biodiversity consequences of natural patterns of intraspecific genetic variation within the widely distributed Australian forest tree, Eucalyptus globulus. We assessed genetic variation among geographic races of E. globulus (i.e., provenances, seed zones) in the characteristics of tree-trunk bark in a 17-year-old common garden and the associated response of a dependent macroarthropod community. In total, 180 macroarthropod taxa were identified following a collection from 100 trees of five races. We found substantial genetically based variation within E. globulus in the quantity and type of decorticating bark. In the community of organisms associated with this bark, significant variation existed among trees of different races in composition, and there was a two-fold difference in species richness (7-14 species) and abundance (22-55 individuals) among races. This community variation was tightly linked with genetically based variation in bark, with 60% of variation in community composition driven by bark characteristics. No detectable correlation was found, however, with neutral molecular markers. These community-level effects of tree genetics are expected to extend to higher trophic levels because of the extensive use of tree trunks as foraging zones by birds and marsupials. Our results demonstrate the potential biodiversity benefits that may be gained through conservation of intraspecific genetic variation within broadly distributed foundation species. The opportunities for enhancing biodiversity values of forestry and restoration plantings are also highlighted because such planted forests are increasingly becoming the dominant forest type in many areas of the world.

Relative importance of tree genetics and microhabitat on macrofungal biodiversity on coarse woody debris.

Understanding the contribution of genetic variation within foundation species to community-level pattern and diversity represents the cornerstone of the developing field of community genetics. We assessed the relative importance of intraspecific genetic variation, spatial variation within a forest and microhabitat variation on a macrofungal decay community developing on logs of the Australian forest tree, Eucalyptus globulus. Uniform logs were harvested from trees from eight geographic races of E. globulus growing in a 15-year-old genetic trial. Logs were placed as designed grids within a native E. globulus forest and after 3 years of natural colonisation the presence of 62 macrofungal taxa were recorded from eight microhabitats on each log. The key factor found to drive macrofungal distribution and biodiversity on structurally uniform coarse woody debris was log-microhabitat, explaining 42% of the total variation in richness. Differences between log-microhabitats appeared to be due to variation in aspect, substrate (bark vs wood) and area/time of exposure to colonisation. This findings demonstrates the importance of considering fine-scale (within substrate) variation in the conservation and management of macrofungal biodiversity, an area that has received little previous attention. While a number of recent studies have demonstrated that the genetics of foundation tree species can influence dependent communities, this was not found to be the case for the early log decay community associated with E. globulus. Despite genetic variation in wood and bark properties existing within this species, there was no significant effect of tree genetics on macrofungal community richness or composition. This finding highlights the variation that may exist among guilds of organisms in their response to genetic variation within foundation species, an important consideration in a promising new area of research.

Genetic variation in resistance of Eucalyptus globulus to marsupial browsers.

The evolution of plant defensive traits in response to selection pressures imposed by herbivores is central to co-evolutionary theory. To demonstrate the role of herbivores as selective agents on plant resistance there must be variability in plant resistance to herbivores within a plant population. This variability must be under genetic control, and the variability in plant resistant traits and consequently herbivore damage to plants must reflect variability in plant fitness. We used a common eucalypt species, Eucalyptus globulus, and two major mammalian herbivores, the common brushtail possum (Trichosurus vulpecula) and the red-bellied pademelon (Thylogale billardierii), as a system to investigate intraspecific variation in plant resistance to mammalian herbivores and to investigate if this variation has a genetic basis. We measured mammalian browsing damage on 2,302 individual trees of E. globulus, from 563 families derived from range-wide native stand seed collections of known pedigree and grown in a common environment field trial. Using a selection of trees from the field trial we then conducted a feeding trial with captive herbivores to assess if the genetic variation in plant resistance in the field was reflected in feeding preferences of captive animals, as measured by relative intake. Results from the field trial showed significant genetic variation in plant resistance amongst races, localities and amongst different families. These results were consolidated in the captive trial with similar trends in genetic variation among E. globulus localities. Dry matter intake of foliage by Trichosurus vulpecula was consistently greater than that by Thylogale billardierii; however, the intraspecific preferences of the two herbivores were significantly correlated.

An AFLP marker approach to lower-level systematics in Eucalyptus (Myrtaceae).

Genus Eucalyptus, with over 700 species, presents a number of systematic difficulties including taxa that hybridize or intergrade across environmental gradients. To date, no DNA marker has been found capable of resolving phylogeny below the sectional level in the major subgenera. Molecular markers are needed to support taxonomic revision, assess the extent of genetic divergence at lower taxonomic levels, and inform conservation efforts. We examined the utility of 930 amplified fragment length polymorphisms (AFLPs) for analyzing relationships among Tasmanian taxa of subgenus Symphyomyrtus section Maidenaria. Phenetic and cladistic analyses resolved species into clusters demonstrating significant genetic partitioning, largely concordant with series defined in the most recent taxonomic revision of Eucalyptus. Some departures from current taxonomy were noted, indicating possible cases of morphological convergence and character reversion. Although the resolution obtained using AFLP was greatly superior to that of single sequence markers, the data demonstrated high homoplasy and incomplete resolution of closely related species. The results of this study and others are consistent with recent speciation and reticulate evolution in Maidenaria. We conclude that a combination of phylogenetic and population genetic approaches using multiple molecular markers offers the best prospects for understanding taxonomic relationships below the sectional level in Eucalyptus.

HYBRIDIZATION AS A DISPERSAL MECHANISM.

An example from the genus Eucalyptus is used to argue that hybridization may be of evolutionary significance as a means of gene dispersal where seed dispersal is limited. A previous study of regeneration of E. risdonii and E. amygdalina indicated that the current selective regime was favoring E. risaonii. However, the dispersal of E. risdonii by seeds is shown to be limited (s, = 4.6 m). By comparison, the flow of E. risdonii genes into the range of E. amygdalina by pollen dispersal and F1 hybridization is widespread (sp = 82 m). While the actual level of hybridization is low, interspecific hybridization effectively doubles the dispersal of E. risdonii genes into the range of E. amygdalina. This pollen flow can have a significant genetic impact, since isolated hybrids or patches of abnormal phenotypes have been found 200-300 m from the species boundary. Based on lignotuber size, some of these patches appear to have been founded by F1 hybrids. The frequency of E. risdonii types in the patches appears to increase with patch size suggesting that there is selection for this phenotype in subsequent generations. E. risdonii-like individuals were recovered in the progeny from both intermediate and E. risdonii backcross phenotypes. These results suggest that E. risdonii may invade suitable habitat islands within the E. amygdalina forest, independently of seed migration, by long-distance pollen migration followed by selection for the gene combinations of the pollen parent.

POSTDISPERSAL SELECTION FOLLOWING MIXED MATING IN EUCALYPTUS REGNANS.

Eucalyptus regnans is a mass flowering, tall forest tree of southeastern Australia with a mixed mating system. A field trial containing randomized single tree plots of self, outcross, and naturally open-pollinated (OP) progenies of 13 parents from two natural populations was surveyed over 15 yr. Inbreeding depression in survival at 15 years was 67% for selfs, one of the highest levels reported for a tree species, and differed little between populations. OP progenies were intermediate and the difference in fitness among the three cross types indicated that at planting, 59% were derived from outcrossing. However, with selection against the inbred progenies, this increased to 83% by 15 yr of age. Most selection against selfs occurred after four years, coincident with canopy closure and the apparent onset of intense competition.

THE RELATIONSHIP BETWEEN CROSS SUCCESS AND SPATIAL PROXIMITY OF EUCALYPTUS GLOBULUS SSP. GLOBULUS PARENTS.

The genetic structure of Eucalyptus globulus forest was examined using progeny vigor as an indirect measure of parental relatedness. Seven trees were crossed with pollen from trees: 0 m (seifing); 21 m (nearest flowering neighbors), 250 m, 500 m, 1 km, 10 km, and 100 km away from the female. Only selfing depressed seed set. Growth of the 21 m progenies was intermediate to selfing and the longer distance pollinations, suggesting tight family clusters occur due to limited seed dispersal. Under this structure biparental inbreeding may be common, however, the cumulative impact of inbreeding seems negligible as relatedness did not appear to decline with distance between mates beyond 50 m.