David Boshier

Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees

The theoretical impacts of anthropogenic habitat degradation on genetic resources have been well articulated. Here we use a simulation approach to assess the magnitude of expected genetic change, and review 31 studies of 23 neotropical tree species to assess whether empirical case studies conform to theory. Major differences in the sensitivity of measures to detect the genetic health of degraded populations were obvious. Most studies employing genetic diversity (nine out of 13) found no significant consequences, yet most that assessed progeny inbreeding (six out of eight), reproductive output (seven out of 10) and fitness (all six) highlighted significant impacts. These observations are in line with theory, where inbreeding is observed immediately following impact, but genetic diversity is lost slowly over subsequent generations, which for trees may take decades. Studies also highlight the ecological, not just genetic, consequences of habitat degradation that can cause reduced seed set and progeny fitness. Unexpectedly, two studies examining pollen flow using paternity analysis highlight an extensive network of gene flow at smaller spatial scales (less than 10 km). Gene flow can thus mitigate against loss of genetic diversity and assist in long-term population viability, even in degraded landscapes. Unfortunately, the surveyed studies were too few and heterogeneous to examine concepts of population size thresholds and genetic resilience in relation to life history. Future suggested research priorities include undertaking integrated studies on a range of species in the same landscapes; better documentation of the extent and duration of impact; and most importantly, combining neutral marker, pollination dynamics, ecological consequences, and progeny fitness assessment within single studies.

Increased pollen flow counteracts fragmentation in a tropical dry forest: An example from Swietenia humilis Zuccarini

Habitat destruction and the resultant fragmentation of the remaining forest are a common phenomenon in the tropics. Most investigations emphasize the potential dangers of fragmentation in isolating patches of forest and exposing populations to loss of species diversity through founder effects, genetic drift, inbreeding, and restricted gene flow. However, a limited number of studies have shown that gene flow may be extensive in tropical trees, suggesting that it may occur between forest fragments and also “isolated” remnant trees. There is an urgent need to quantify pollen flow within and between forest fragments to test the veracity of such views and determine the genetic value of such fragments for in situ conservation. Microsatellite markers are used to genotype individuals of Swietenia humilis from a highly fragmented forest mosaic to directly quantify pollen-mediated gene flow. Distances of pollen flow more than 10 times greater than previously reported were detected. Our results show that some tropical angiosperm tree species may be much more adaptable and resilient to habitat destruction and fragmentation than previously considered. The description of many remnant trees as isolated or “living dead” may be more a conditioning of human perception than a true reflection of their potential conservation value.

Genetic variation within a fragmented population of Swietenia humilis Zucc.

With large tracts of once continuous forest now modified by human use to leave reduced and highly fragmented stands of trees, the determination of the genetic consequences of forest fragmentation is a priority for ascertaining the conservation value of resultant stands, and in formulating sustainable management strategies. The levels and distribution of genetic diversity over 10 microsatellite loci were investigated within a fragmented population of the neotropical tree Swietenia humilis Zucc. High levels of genetic variation, typical of a highly outcrossing species, were found in all fragments at all loci (mean HE = 0.548). The majority of the variation was within rather than between fragments (RST = 0.032), giving high indirect estimates of gene flow (Nm = 8.9), probably reflecting the genetic structure of the trees present under more continuous forest. A high proportion of loci also showed significant departures from Hardy–Weinberg equilibrium with associated significant levels of FIS. The initial effects of fragmentation were, however, seen in the fragments through the loss of low‐frequency alleles present in the continuous ‘control’ stand. The percentage of this allelic loss increased with a decrease in fragment size.

Population genetics of Cordia alliodora (Boraginaceae), a neotropical tree. 2. Mating system.

A multilocus mixed mating model was used to evaluate the mating system of a natural population of Cordia alliodora (Boraginaceae), a neotropical tree. The population was highly outcrossed (tin = 0.966 ? 0.027), in agreement with results from controlled crosses. Departures from the mixed mating model were evident, suggesting some nonrandom, correlated mating. Pollen pool heterogeneity and variation in estimates of individual outcrossing rates indicated that the population may be genetically substructured. Individual outcrossing rates obtained for the samples taken from within different parts of the same tree indicated reduced levels of outcrossing due to limited sampling of the pollen pool. The incompatibility mechanism in C. alliodora, combined with variation in flowering and stand density, appears to lead to both temporal and spatial substructuring of the population.

Ecology provides a pragmatic solution to the maintenance of genetic diversity in sustainably managed tropical rain forests

Abstract An important aspect of the sustainable management of tropical rain forests is the maintenance of genetic diversity within populations of commercial tree species. Logging may reduce genetic variation directly and may also affect genetic processes, leading possibly to genetic erosion and ultimately even species extinction. It is, however, impractical for the forest manager to make meaningful measurements of genetic variation and they are therefore inappropriate for use as indicators of sustainable forest management. We propose that the application of well-known silvicultural principles is the most practical way of preventing rapid loss of genetic diversity. Most tropical rain forest tree species have many more individuals below the minimum size for commercial exploitation than above. The genetic diversity of these species will be little affected by logging, as the stems removed form only a small fraction of the total population. Similarly, for most species, disruption of normal mating patterns will either not occur or be transient, because reproduction commences at sizes well below felling limits, or because, after logging, juveniles will be recruited to the sexually mature size classes. Strongly light-demanding species with a commercial value are most likely to suffer loss of genetic diversity from logging. Characteristically, these have populations in which only a small proportion of the total population lies in small size classes. In order to conserve genetic diversity, pre-felling silvicultural treatments will be required to increase the survival and growth of juveniles. Ecological and genetic research needs to focus on these light-demanding species.

Genome sequence and genetic diversity of European ash trees

Ash trees (genus Fraxinus, family Oleaceae) are widespread throughout the Northern Hemisphere, but are being devastated in Europe by the fungus Hymenoscyphus fraxineus, causing ash dieback, and in North America by the herbivorous beetle Agrilus planipennis. Here we sequence the genome of a low-heterozygosity Fraxinus excelsior tree from Gloucestershire, UK, annotating 38,852 protein-coding genes of which 25% appear ash specific when compared with the genomes of ten other plant species. Analyses of paralogous genes suggest a whole-genome duplication shared with olive (Olea europaea, Oleaceae). We also re-sequence 37 F. excelsior trees from Europe, finding evidence for apparent long-term decline in effective population size. Using our reference sequence, we re-analyse association transcriptomic data, yielding improved markers for reduced susceptibility to ash dieback. Surveys of these markers in British populations suggest that reduced susceptibility to ash dieback may be more widespread in Great Britain than in Denmark. We also present evidence that susceptibility of trees to H. fraxineus is associated with their iridoid glycoside levels. This rapid, integrated, multidisciplinary research response to an emerging health threat in a non-model organism opens the way for mitigation of the epidemic.

The resilience of forest fragmentation genetics—no longer a paradox—we were just looking in the wrong place

The resilience of forest fragmentation genetics—no longer a paradox—we were just looking in the wrong place

Aquaporins in the wild: natural genetic diversity and selective pressure in the PIP gene family in five Neotropical tree species.

BackgroundTropical trees undergo severe stress through seasonal drought and flooding, and the ability of these species to respond may be a major factor in their survival in tropical ecosystems, particularly in relation to global climate change. Aquaporins are involved in the regulation of water flow and have been shown to be involved in drought response; they may therefore play a major adaptive role in these species. We describe genetic diversity in the PIP sub-family of the widespread gene family of Aquaporins in five Neotropical tree species covering four botanical families.ResultsPIP Aquaporin subfamily genes were isolated, and their DNA sequence polymorphisms characterised in natural populations. Sequence data were analysed with statistical tests of standard neutral equilibrium and demographic scenarios simulated to compare with the observed results. Chloroplast SSRs were also used to test demographic transitions. Most gene fragments are highly polymorphic and display signatures of balancing selection or bottlenecks; chloroplast SSR markers have significant statistics that do not conform to expectations for population bottlenecks. Although not incompatible with a purely demographic scenario, the combination of all tests tends to favour a selective interpretation of extant gene diversity.ConclusionsTropical tree PIP genes may generally undergo balancing selection, which may maintain high levels of genetic diversity at these loci. Genetic variation at PIP genes may represent a response to variable environmental conditions.

Remnant Pachira quinata pasture trees have greater opportunities to self and suffer reduced reproductive success due to inbreeding depression

Habitat fragmentation is extensive throughout the world, converting natural ecosystems into fragments of varying size, density and connectivity. The potential value of remnant trees in agricultural landscapes as seed sources and in connecting fragments has formed a fertile area of debate. This study contrasted the mating patterns of bat-pollinated Pachira quinata trees in a continuous forest to those in pasture through microsatellite-based paternity analysis of progeny. The breeding system was determined by analysis of pollen tube growth and seed production from controlled pollinations. Fitness of selfed and outcrossed seed was compared by germination and seedling growth. There was more inbreeding within pasture trees (outcrossing=0.828±0.015) compared with forest trees (0.926±0.005). Pasture trees had fewer sires contributing to mating events, but pollen dispersal distances were greater than those in the forest. Paternity analysis showed variation in outcrossing rates among pasture trees with high proportions of external and self pollen sources detected. A leaky self-incompatibility system was found, with self pollen having reduced germination on stigmas and slower growth rate through the style. Controlled pollinations also showed a varied ability to self among trees, which was reflected in the selfing rates among pasture trees shown by the paternity analysis (0–80% selfing). Self pollination resulted in lower seed set, germination and seedling growth compared with outcrossing. While remnant trees in agricultural landscapes are involved in broader mating patterns, they show increased but varied levels of inbreeding, which result in reduced fitness.

Is local best? Examining the evidence for local adaptation in trees and its scale

BackgroundAlthough the importance of using local provenance planting stock for woodland production, habitat conservation and restoration remains contentious, the concept is easy to understand, attractive and easy to ‘sell’. With limited information about the extent and scale of adaptive variation in native trees, discussion about suitable seed sources often emphasises “local” in a very narrow sense or within political boundaries, rather than being based on sound evidence of the scale over which adaptation occurs. Concerns exist over the actual scale (magnitude and spatial scale) of adaptation in trees and the relative dangers of incorrect seed source or restricted seed collection, leading to the establishment of trees with restricted genetic diversity and limited adaptive potential. Tree provenance and progeny field trials in many parts of the world have shown the existence of genotype by environment interaction in many tree species, but have not necessarily looked at whether this is expressed as a home site advantage (i.e. whether provenance performance is unstable across sites, and there is better performance of a local seed source).Methods/designThis review will examine the evidence for local adaptation and its scale in a number of native tree species from different trial sites across the globe (e.g. tropical, Mediterranean, temperate). These trials have been measured and in some cases results published in a range of formats. The data have, however, usually been presented in the form of which provenances grow best at which sites. The review will examine existing data (published and unpublished) in the context of the scale of local adaptation, with the results being presented in two formats: (a) relating survival, performance of provenances (classified by seed zone/provenance region of origin) to seed zone/provenance region of the planting site; (b) plotting survival, performance provenances against the distance (Euclidean/ecological) between the provenance and the trial site.