Short-term genetic consequences of habitat loss and fragmentation for the neotropical palm Oenocarpus bataua.

Habitat loss and fragmentation may impact animal-mediated dispersal of seed and pollen, and a key question is how the genetic attributes of plant populations respond to these changes. Theory predicts that genetic diversity may be less sensitive to such disruptions in the short term, whereas inbreeding and genetic structure may respond more strongly. However, results from studies to date vary in relation to species, context and the parameter being assessed, triggering calls for more empirical studies, especially from the tropics, where plant-animal dispersal mutualisms are both disproportionately common and at risk. We compared the genetic characteristics of adults and recruits in a long-lived palm Oenocarpus bataua in a recently fragmented landscape (<2 generations) in northwest Ecuador using a suite of 10 polymorphic microsatellite markers. We sampled individuals from six forest fragments and one nearby continuous forest. Our goal was to assess short-term consequences of fragmentation, with a focus on how well empirical data from this system follow theoretical expectations. Mostly congruent with predictions, we found stronger genetic differentiation and fine-scale spatial genetic structure among recruits in fragments compared with recruits in continuous forest, but we did not record differences in genetic diversity or inbreeding, nor did we record any differences between adults in fragments and adults in continuous forest. Our findings suggest that genetic characteristics of populations vary in their sensitivity to change in response to habitat loss and fragmentation, and that fine-scale spatial genetic structure may be a particularly useful indicator of genetic change in recently fragmented landscapes.

Mating patterns and pollinator mobility are critical traits in forest fragmentation genetics.

Most woody plants are animal-pollinated, but the global problem of habitat fragmentation is changing the pollination dynamics. Consequently, the genetic diversity and fitness of the progeny of animal-pollinated woody plants sired in fragmented landscapes tend to decline due to shifts in plant-mating patterns (for example, reduced outcrossing rate, pollen diversity). However, the magnitude of this mating-pattern shift should theoretically be a function of pollinator mobility. We first test this hypothesis by exploring the mating patterns of three ecologically divergent eucalypts sampled across a habitat fragmentation gradient in southern Australia. We demonstrate increased selfing and decreased pollen diversity with increased fragmentation for two small-insect-pollinated eucalypts, but no such relationship for the mobile-bird-pollinated eucalypt. In a meta-analysis, we then show that fragmentation generally does increase selfing rates and decrease pollen diversity, and that more mobile pollinators tended to dampen these mating-pattern shifts. Together, our findings support the premise that variation in pollinator form contributes to the diversity of mating-pattern responses to habitat fragmentation.

Mating system and early viability resistance to habitat fragmentation in a bird-pollinated eucalypt.

Habitat fragmentation has been shown to disrupt ecosystem processes such as plant-pollinator mutualisms. Consequently, mating patterns in remnant tree populations are expected to shift towards increased inbreeding and reduced pollen diversity, with fitness consequences for future generations. However, mating patterns and phenotypic assessments of open-pollinated progeny have rarely been combined in a single study. Here, we collected seeds from 37 Eucalyptus incrassata trees from contrasting stand densities following recent clearance in a single South Australian population (intact woodland=12.6 trees ha(-1); isolated pasture=1.7 trees ha(-1); population area=10 km(2)). 649 progeny from these trees were genotyped at eight microsatellite loci. We estimated genetic diversity, spatial genetic structure, indirect contemporary pollen flow and mating patterns for adults older than the clearance events and open-pollinated progeny sired post-clearance. A proxy of early stage progeny viability was assessed in a common garden experiment. Density had no impact on mating patterns, adult and progeny genetic diversity or progeny growth, but was associated with increased mean pollen dispersal. Weak spatial genetic structure among adults suggests high historical gene flow. We observed preliminary evidence for inbreeding depression related to stress caused by fungal infection, but which was not associated with density. Higher observed heterozygosities in adults compared with progeny may relate to weak selection on progeny and lifetime-accumulated mortality of inbred adults. E. incrassata appears to be resistant to the negative mating pattern and fitness changes expected within fragmented landscapes. This pattern is likely explained by strong outcrossing and regular long-distance pollen flow.

Is the post-disturbance composition of a plant population determined by selection for outcrossed seedlings or by the composition of the seedbank?

Seedbanks are expected to buffer populations against disturbances, such as fire, that could alter the genetic composition of smaller, ephemeral adult populations. However, seedling genotypes may be influenced by the spatially heterogeneous nature of both the seedbank and the disturbance (for example, germination may vary with local disturbance) and also by selection acting on germination and post-germination performance. We used microsatellite-DNA surveys of seedlings emerging from the soil-stored seedbanks of Grevillea macleayana after wildfire to compare diversity and spatial structure in seedlings and adults, and through resampling of the seedling data set, to determine whether the resultant adult population reflected the effects of selection or random seedling mortality. The large post-fire seedling cohorts captured the full allelic diversity of the pre-fire adult population. However, we found a mismatch in the genotypic structure of adults and seedlings. Seedlings displayed larger heterozygous deficits than adults; however, over the ensuing 11 years, seedling heterozygosity eventually matched values for the pre-fire adults. Increasing heterozygosity among adults has generally been attributed to heterosis and/or reduction in Wahlund effects via self-thinning. Resampling of early post-fire seedlings to generate samples of equivalent size to survivors at 11 years showed that increases in heterozygosity must be driven by selection favouring outcrossed seed. This finding is important in an evolutionary context but also has implications for the restoration of natural or managed populations where a seedbank is a viable source of recruits.

The pollen dispersal kernel and mating system of an insect-pollinated tropical palm, Oenocarpus bataua.

Pollen dispersal shapes the local genetic structure of plant populations and determines the opportunity for local selection and genetic drift, but has been well studied in few animal-pollinated plants in tropical rainforests. Here, we characterise pollen movement for an insect-pollinated Neotropical canopy palm, Oenocarpus bataua, and relate these data to adult mating system and population genetic structure. The study covers a 130-ha parcel in which all adult trees (n=185) were mapped and genotyped at 12 microsatellite loci, allowing us to positively identify the source tree for 90% of pollination events (n=287 of 318 events). Mating system analysis showed O. bataua was effectively outcrossed (t(m)=1.02) with little biparental inbreeding (t(m)-t(s)=-0.005) and an average of 5.4 effective pollen donors (N(ep)) per female. Dispersal distances were relatively large for an insect-pollinated species (mean=303 m, max=1263 m), and far exceeded nearest-neighbour distances. Dispersal kernel modelling indicated a thin-tailed Weibull distribution offered the best fit to the genetic data, which contrasts with the fat-tailed kernels typically reported for pollen dispersal in trees. Preliminary analyses suggest that our findings may be explained, at least in part, by a relatively diffuse spatial and temporal distribution of flowering trees. Comparison with previously reported estimates of seed movement for O. bataua suggests that pollen and seed dispersal distances may be similar. These findings add to the growing body of information on dispersal in insect-pollinated trees, but underscore the need for continued research on tropical systems in general, and palms in particular.

Multiplexed microsatellite markers for the genetic analysis of Eucalyptus leucoxylon (Myrtaceae) and their utility for ecological and breeding studies in other eucalyptus species.

Eucalyptus leucoxylon is a widespread woodland tree species found in southeastern Australia that has suffered from, and continues to be, threatened by the impacts of habitat clearance and degradation. Populations now consist predominantly of scattered individuals, and their conservation status is of increasing concern. We report the development and characterization of a set of eight highly polymorphic microsatellite loci for E. leucoxylon. The loci can be amplified in three PCR multiplexes and electrophoresed in a single lane, allowing rapid throughput of large numbers of samples. A total of 111 alleles were detected in 68 individuals with an average of 12.3 alleles per locus, a mean expected heterozygosity of 0.83, and a mean observed heterozygosity of 0.72. The combined probabilities of identity and probabilities of paternity exclusion allow an extremely precise level of individual identification, indicating that these microsatellite markers will be ideal for population genetic and parentage-type studies in E. leucoxylon. The markers also exhibited an average of 76% conservation within the subgenus Symphyomyrtus, to which E. leucoxylon belongs, and 53% conservation across other subgenera of Eucalyptus, demonstrating the potential of these markers in ecological and breeding studies in a wide range of Eucalyptus species.