The patterns of hybridization and asymmetrical gene flow among species are important for understanding the processes that maintain distinct species. We examined the potential for asymmetrical gene flow in sympatric populations of Eucalyptus aggregata and Eucalyptus rubida, both longlived trees of southern Australia. A total of 421 adults from three hybrid zones were genotyped with six microsatellite markers. We used genealogical assignments, admixture analysis and analyses of spatial genetic structure and spatial distribution of individuals, to assess patterns of interspecific gene flow within populations. A high number of admixed individuals were detected (13.9-40% of individuals), with hybrid populations consisting of F 1 and F 2 hybrids and backcrosses in both parental directions. Across the three sites, admixture proportions were skewed towards the E. aggregata genetic cluster (x ¼ 0.56-0.65), indicating that backcrossing towards E. aggregata is more frequent. Estimates of long-term migration rates also indicate asymmetric gene flow, with higher migration rates from E. aggregata to hybrids compared with E. rubida. Taken together, these results indicate a greater genetic input from E. aggregata into the hybrid populations. This asymmetry probably reflects differences in style lengths (E. rubida: B7 mm, E. aggregata: B4 mm), which can prevent pollen tubes of smaller-flowered species from fertilizing larger-flowered species. However, analyses of fine-scale genetic structure suggest that localized seed dispersal (o40 m) and greater clustering between hybrid and E. aggregata individuals may also contribute to directional gene flow. Our study highlights that floral traits and the spatial distributions of individuals can be useful predictors of the directionality of interspecific gene flow in plant populations.
Introductions of European honeybees have occurred globally, potentially affecting the natural pollination ecology of many plants. Introduced honeybees are now the most frequent visitors to the inflorescences of the self‐compatible, bird‐pollinated Australian shrub Grevillea macleayana and may therefore be expected to have altered the mating system. To examine the degree to which birds continue to play a role in determining the mating system of G. macleayana in this disturbed system, we compared outcrossing rates in open‐pollinated inflorescences with inflorescences from which birds had been selectively excluded. Outcrossing rates were estimated from the microsatellite genotypes of over 100 seeds per population in three populations. Outcrossing rates ( t) in open‐pollinated seeds were surprisingly low (0.062–0.225) and did not vary significantly among the three populations. Nevertheless, outcrossing was significantly lower when birds were excluded (data pooled from all populations). Two lines of evidence suggest that there are temporal fluctuations in outcrossing rate and hence that birds usually have a major effect on the mating system of G. macleayana. First, at one site, t was substantially lower than estimates from an earlier study (0.06 in 1995 cf. 0.85 in 1990). Second, fixation indices based on seeds were high in all populations ( >0.68), whereas values for the established plants ( parental generation) were much lower in two of the three populations (0.06–0.32). Our findings suggest that honeybee activity is so high that the contribution of birds to pollination in G. macleayana is sometimes relatively trivial.
Recent habitat loss and fragmentation superimposed upon ancient patterns of population subdivision are likely to have produced low levels of neutral genetic diversity and marked genetic structure in many plant species. The genetic effects of habitat fragmentation may be most pronounced in species that form small populations, are fully self-compatible and have limited seed dispersal. However, long-lived seed banks, mobile pollinators and long adult lifespans may prevent or delay the accumulation of genetic effects. We studied a rare Australian shrub species, Grevillea macleayana (Proteaceae), that occurs in many small populations, is self-compatible and has restricted seed dispersal. However, it has a relatively long adult lifespan (c. 30 years), a long-lived seed bank that germinates after fire and is pollinated by birds that are numerous and highly mobile. These latter characteristics raise the possibility that populations in the past may have been effectively large and genetically homogeneous. Using six microsatellites, we found that G. macleayana may have relatively low within-population diversity (3.2-4.2 alleles/locus; Hexp = 0.420-0.530), significant population differentiation and moderate genetic structure (FST = 0.218) showing isolation by distance, consistent with historically low gene flow. The frequency distribution of allele sizes suggest that this geographical differentiation is being driven by mutation. We found a lack mutation-drift equilibrium in some populations that is indicative of population bottlenecks. Combined with evidence for large spatiotemporal variation of selfing rates, this suggests that fluctuating population sizes characterize the demography in this species, promoting genetic drift. We argue that natural patterns of pollen and seed dispersal, coupled with the patchy, fire-shaped distribution, may have restricted long-distance gene flow in the past.
The genetic effects of population fragmentation cannot be interpreted without understanding the underlying pattern of genetic variation resulting from historic population processes. We used AFLP markers to determine genetic structure and distribution of genetic diversity among populations of an endangered Australian shrub Grevillea caleyi (Proteaceae). Populations that occurred historically on four ridges have new been fragmented to varying degrees, producing some large, relatively pristine populations and very small populations consisting of fewer than 10 adult plants. We found marked population genetic structure (65.9% of genetic variation was among populations) and a significant relationship between genetic and geographic distance (r m ¼ 0.564, P ¼ 0.004). However, only 14% of overall genetic differentiation was attributable to variation among ridges, compared with 52% among populations within ridges. Moreover, genetic diversity within samples of plants did not vary with either population size or degree of isolation. Thus, the present genetic structure of populations is probably almost entirely the product of historical events. Fine-scale structuring within populations prior to fragmentation may have been caused by limited seed and pollen dispersal, despite a complex suite of (mostly avian) pollinators, and a mixed mating system that allows a large amount of selfing. The combined effects of adult longevity and a soil-stored seed bank may have buffered the recently fragmented populations against the effects of dramatic reductions in numbers of adult plants.
Ecotones have been considered as unique environments, and the concepts of edge effect and ecotonal species have been widely used, especially in avian community ecology. We studied the patterns of bird densities across heath-wood edges at replicated sites in three locations in southeastern Australia. Multivariate analysis showed that the bird community in the ecotone was intermediate between the heath and wood communities, indicating that the ecotone contained a mixing of species rather than a unique bird community. ANOVA showed a modest increase in bird density at the wood side of the ecotone, which may be partly due to sampling biases rather than to some inherent habitat value in the ecotone. The outstanding pattern was that bird density and species richness in the wood habitat were twice as high as in the heath habitat. Of a total of 86 species, 31 occurred in sufficient numbers to categorize according to their habitat association (generalist, or heath or wood specialist) and their density at the ecotone (ecotone neutral, ecotone shy, or ecotone conspicuous). Three of these were habitat-generalist-ecotone-neutral. Fourteen species were ecotone neutral but were habitat specialists on either the wood (13 spp.) or the heath (1 sp.). Three species were ecotone shy. Although 11 species were ecotone conspicuous, they also occurred in either heath or wood or both. Thus, no species could be categorized as entirely ecotonal. We conclude that there is little evidence from this or other studies of avian communities to support an edge effect of increased density and species richness, and no evidence of entirely ecotonal species.
Experimental hand pollinations have revealed that the Australian proteaceous shrub Grevillea barklyana is fully self-compatible, although one study suggested that when both self-and outcross pollen were presented to different flowers on the same inflorescence significantly greater seed set resulted from the outcrossed flowers. This study used single-locus electrophoretic surveys of maternal plants and their progeny arrays to test the prediction that this apparent 'preference' for outcross pollen would produce high levels of outcrossing within natural populations. We found instead that plants within three of four populations were almost completely selfed. Outcrossing rates (t) in each of these populations (based on the progeny arrays of a minimum of nine plants) ranged from 0.07 0.03 to only 0.33 0.08 and showed little variation among years, ranging from 0.07 0.03 to 0.10 0.03 for a population sampled in each of two breeding seasons. Furthermore, examination of the progeny arrays from plants in the most intensively studied population revealed virtually no exchange of genes between immediately adjacent plants. Three pairs of alternative homozygotes were near neighbours (separated by less than 2 m) and yet detectable outcrosses comprised only seven of the 108 seeds sampled. In contrast, the fourth population of G. barklyana appeared highly outcrossed (t =0.85±0.2) which is typical of the realized mating system reported for other Australian Proteaceae. These data show that the realized mating system may vary widely among populations and may often be less than optimal. The occurrence of very low outcrossing rates within some populations may reflect the presence of introduced pollinators or other disturbances.
The frequency of hybridization in plants is context dependent and can be influenced by the local mating environment. We used progeny arrays and admixture and pollen dispersal analyses to assess the relative importance of pre-mating reproductive barriers and the local demographic environment as explanations of variation in hybrid frequency in three mapped hybrid zones of Eucalyptus aggregata and E. rubida. A total of 731 open-pollinated progeny from 36 E. aggregata maternal parents were genotyped using six microsatellite markers. Admixture analysis identified substantial variation in hybrid frequency among progeny arrays (0-76.9%). In one hybrid zone, hybrid frequency was related to pre-mating barriers (degree of flowering synchrony) and demographic components of the local mating environment (decreasing population size, closer proximity to E. rubida and hybrid trees). At this site, average pollen dispersal distance was less and almost half (46%) of the hybrid progeny were sired by local E. rubida and hybrid trees. In contrast, at the other two sites, pre-mating and demographic factors were not related to hybrid frequency. Compared to the first hybrid zone where most of the E. rubida (76%) and all hybrids flowered, in the remaining sites fewer E. rubida (22-41%) and hybrid trees (0-50%) flowered and their reproductive success was lower (sired 0-23% of hybrids). As a result, most hybrids were sired by external E. rubida/hybrids located at least 2-3 km away. These results indicate that although pre-mating barriers and local demography can influence patterns of hybridization, their importance can depend upon the scale of pollen dispersal.
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