Evolution of endemism on a young tropical mountain.

Tropical mountains are hot spots of biodiversity and endemism, but the evolutionary origins of their unique biotas are poorly understood. In varying degrees, local and regional extinction, long-distance colonization, and local recruitment may all contribute to the exceptional character of these communities. Also, it is debated whether mountain endemics mostly originate from local lowland taxa, or from lineages that reach the mountain by long-range dispersal from cool localities elsewhere. Here we investigate the evolutionary routes to endemism by sampling an entire tropical mountain biota on the 4,095-metre-high Mount Kinabalu in Sabah, East Malaysia. We discover that most of its unique biodiversity is younger than the mountain itself (6 million years), and comprises a mix of immigrant pre-adapted lineages and descendants from local lowland ancestors, although substantial shifts from lower to higher vegetation zones in this latter group were rare. These insights could improve forecasts of the likelihood of extinction and 'evolutionary rescue' in montane biodiversity hot spots under climate change scenarios.

Incorporating connectivity into conservation planning for the optimal representation of multiple species and ecosystem services.

Conservation planning tends to focus on protecting species' ranges or landscape connectivity but seldom both-particularly in the case of diverse taxonomic assemblages and multiple planning goals. Therefore, information on potential trade-offs between maintaining landscape connectivity and achieving other conservation objectives is lacking. We developed an optimization approach to prioritize the maximal protection of species' ranges, ecosystem types, and forest carbon stocks, while also including habitat connectivity for range-shifting species and dispersal corridors to link protected area. We applied our approach to Sabah, Malaysia, where the state government mandated an increase in protected-area coverage of approximately 305,000 ha but did not specify where new protected areas should be. Compared with a conservation planning approach that did not incorporate the 2 connectivity features, our approach increased the protection of dispersal corridors and elevational connectivity by 13% and 21%, respectively. Coverage of vertebrate and plant species' ranges and forest types were the same whether connectivity was included or excluded. Our approach protected 2% less forest carbon and 3% less butterfly range than when connectivity features were not included. Hence, the inclusion of connectivity into conservation planning can generate large increases in the protection of landscape connectivity with minimal loss of representation of other conservation targets.

Incorporación de la Conectividad a la Planeación de la Conservación para la Representación Óptima de Especies Múltiples y Servicios Ambientales Resumen Las tendencias de planeación de la conservación tienden a enfocarse en la protección de la distribución geográfica de las especies o en la conectividad de paisajes, pero rara vez se enfocan en ambas - particularmente para el caso de los ensamblajes taxonómicos y las metas múltiples de planeación. Por lo tanto, hay carencias en la información sobre las compensaciones potenciales entre mantener la conectividad de los paisajes y alcanzar otros objetivos de conservación. Desarrollamos una estrategia de optimización para priorizar la protección máxima de la distribución de las especies, los tipos de ecosistemas y los stocks de carbono de los bosques, a la vez que incluimos la conectividad del hábitat para las especies que modifican su distribución y los corredores de dispersión para conectar el área protegida. Aplicamos nuestra estrategia en Sabah, Malasia, en donde el gobierno estatal ordenó un incremento de ∼305, 000 ha en la cobertura de áreas protegidas sin especificar la ubicación de las nuevas áreas protegidas. En comparación con una estrategia de planeación de la conservación que no incorporó las dos características de la conectividad, nuestra estrategia incrementó la protección de los corredores de dispersión y la conectividad altitudinal en un 13% y 21% respectivamente. La cobertura de la distribución de las especies de plantas y vertebrados y de los tipos de bosque fue la misma con o sin la inclusión de la conectividad. Nuestra estrategia protegió 2% menos del carbono forestal y 3% menos de la distribución de mariposas que cuando no se incluyeron las características de conectividad en la estrategia. Por lo tanto, incluir a la conectividad en la planeación de la conservación puede generar grandes incrementos en la protección de la conectividad del paisaje con una pérdida mínima de representación para los demás objetivos de conservación.

Genetic Diversity and Demographic History of an Upper Hill Dipterocarp (Shorea platyclados): Implications for Conservation.

Southeast Asian rainforests at upper hill elevations are increasingly vulnerable to degradation because most lowland forest areas have been converted to different land uses. As such, understanding the genetics of upper hill species is becoming more crucial for their future management and conservation. Shorea platyclados is an important, widespread upper hill dipterocarp in Malaysia. To elucidate the genetic structure of S. platyclados and ultimately provide guidelines for a conservation strategy for this species, we carried out a comprehensive study of the genetic diversity and demographic history of S. platyclados. Twenty-seven populations of S. platyclados across its range in Malaysia were genotyped at 15 polymorphic microsatellite loci and sequenced at seven noncoding chloroplast DNA (cpDNA) regions. A total of 303 alleles were derived from the microsatellite loci, and 29 haplotypes were identified based on 2892 bp of concatenated cpDNA sequences. The populations showed moderately high genetic diversity (mean HE = 0.680 for microsatellite gene diversity and HT = 0.650 for total haplotype diversity) and low genetic differentiation (FST = 0.060). Bayesian clustering divided the studied populations into two groups corresponding to western and eastern Malaysia. Bottleneck analysis did not detect any recent bottleneck events. Extended Bayesian skyline analyses showed a model of constant size for the past population history of this species. Based on our findings, priority areas for in situ and ex situ conservation and a minimum population size are recommended for the sustainable utilization of S. platyclados.

Partitioning of soil phosphorus among arbuscular and ectomycorrhizal trees in tropical and subtropical forests.

Partitioning of soil phosphorus (P) pools has been proposed as a key mechanism maintaining plant diversity, but experimental support is lacking. Here, we provided different chemical forms of P to 15 tree species with contrasting root symbiotic relationships to investigate plant P acquisition in both tropical and subtropical forests. Both ectomycorrhizal (ECM) and arbuscular mycorrhizal (AM) trees responded positively to addition of inorganic P, but strikingly, ECM trees acquired more P from a complex organic form (phytic acid). Most ECM tree species and all AM tree species also showed some capacity to take up simple organic P (monophosphate). Mycorrhizal colonisation was negatively correlated with soil extractable P concentration, suggesting that mycorrhizal fungi may regulate organic P acquisition among tree species. Our results support the hypothesis that ECM and AM plants partition soil P sources, which may play an ecologically important role in promoting species coexistence in tropical and subtropical forests.

Nuclear and chloroplast DNA phylogeography reveals Pleistocene divergence and subsequent secondary contact of two genetic lineages of the tropical rainforest tree species Shorea leprosula (Dipterocarpaceae) in South-East Asia.

Tropical rainforests in South-East Asia have been affected by climatic fluctuations during past glacial eras. To examine how the accompanying changes in land areas and temperature have affected the genetic properties of rainforest trees in the region, we investigated the phylogeographic patterns of a widespread dipterocarp species, Shorea leprosula. Two types of DNA markers were used: expressed sequence tag-based simple sequence repeats and chloroplast DNA (cpDNA) sequence variations. Both sets of markers revealed clear genetic differentiation between populations in Borneo and those in the Malay Peninsula and Sumatra (Malay/Sumatra). However, in the south-western part of Borneo, genetic admixture of the lineages was observed in the two marker types. Coalescent simulation based on cpDNA sequence variation suggested that the two lineages arose 0.28-0.09 million years before present and that following their divergence migration from Malay/Sumatra to Borneo strongly exceeded migration in the opposite direction. We conclude that the genetic structure of S. leprosula was largely formed during the middle Pleistocene and was subsequently modified by eastward migration across the subaerially exposed Sunda Shelf.

Are patterns of fine-scale spatial genetic structure consistent between sites within tropical tree species?

Documenting the scale and intensity of fine-scale spatial genetic structure (FSGS), and the processes that shape it, is relevant to the sustainable management of genetic resources in timber tree species, particularly where logging or fragmentation might disrupt gene flow. In this study we assessed patterns of FSGS in three species of Dipterocarpaceae (Parashorea tomentella, Shorea leprosula and Shorea parvifolia) across four different tropical rain forests in Malaysia using nuclear microsatellite markers. Topographic heterogeneity varied across the sites. We hypothesised that forests with high topographic heterogeneity would display increased FSGS among the adult populations driven by habitat associations. This hypothesis was not supported for S. leprosula and S. parvifolia which displayed little variation in the intensity and scale of FSGS between sites despite substantial variation in topographic heterogeneity. Conversely, the intensity of FSGS for P. tomentella was greater at a more topographically heterogeneous than a homogeneous site, and a significant difference in the overall pattern of FSGS was detected between sites for this species. These results suggest that local patterns of FSGS may in some species be shaped by habitat heterogeneity in addition to limited gene flow by pollen and seed dispersal. Site factors can therefore contribute to the development of FSGS. Confirming consistency in species' FSGS amongst sites is an important step in managing timber tree genetic diversity as it provides confidence that species specific management recommendations based on species reproductive traits can be applied across a species' range. Forest managers should take into account the interaction between reproductive traits and site characteristics, its consequences for maintaining forest genetic resources and how this might influence natural regeneration across species if management is to be sustainable.

Geographic origin and individual assignment of Shorea platyclados (Dipterocarpaceae) for forensic identification.

The development of timber tracking methods based on genetic markers can provide scientific evidence to verify the origin of timber products and fulfill the growing requirement for sustainable forestry practices. In this study, the origin of an important Dark Red Meranti wood, Shorea platyclados, was studied by using the combination of seven chloroplast DNA and 15 short tandem repeats (STRs) markers. A total of 27 natural populations of S. platyclados were sampled throughout Malaysia to establish population level and individual level identification databases. A haplotype map was generated from chloroplast DNA sequencing for population identification, resulting in 29 multilocus haplotypes, based on 39 informative intraspecific variable sites. Subsequently, a DNA profiling database was developed from 15 STRs allowing for individual identification in Malaysia. Cluster analysis divided the 27 populations into two genetic clusters, corresponding to the region of Eastern and Western Malaysia. The conservativeness tests showed that the Malaysia database is conservative after removal of bias from population subdivision and sampling effects. Independent self-assignment tests correctly assigned individuals to the database in an overall 60.60-94.95% of cases for identified populations, and in 98.99-99.23% of cases for identified regions. Both the chloroplast DNA database and the STRs appear to be useful for tracking timber originating in Malaysia. Hence, this DNA-based method could serve as an effective addition tool to the existing forensic timber identification system for ensuring the sustainably management of this species into the future.

Forensic timber identification: a case study of a CITES listed species, Gonystylus bancanus (Thymelaeaceae).

Illegal logging and smuggling of Gonystylus bancanus (Thymelaeaceae) poses a serious threat to this fragile valuable peat swamp timber species. Using G. bancanus as a case study, DNA markers were used to develop identification databases at the species, population and individual level. The species level database for Gonystylus comprised of an rDNA (ITS2) and two cpDNA (trnH-psbA and trnL) markers based on a 20 Gonystylus species database. When concatenated, taxonomic species recognition was achieved with a resolution of 90% (18 out of the 20 species). In addition, based on 17 natural populations of G. bancanus throughout West (Peninsular Malaysia) and East (Sabah and Sarawak) Malaysia, population and individual identification databases were developed using cpDNA and STR markers respectively. A haplotype distribution map for Malaysia was generated using six cpDNA markers, resulting in 12 unique multilocus haplotypes, from 24 informative intraspecific variable sites. These unique haplotypes suggest a clear genetic structuring of West and East regions. A simulation procedure based on the composition of the samples was used to test whether a suspected sample conformed to a given regional origin. Overall, the observed type I and II errors of the databases showed good concordance with the predicted 5% threshold which indicates that the databases were useful in revealing provenance and establishing conformity of samples from West and East Malaysia. Sixteen STRs were used to develop the DNA profiling databases for individual identification. Bayesian clustering analyses divided the 17 populations into two main genetic clusters, corresponding to the regions of West and East Malaysia. Population substructuring (K=2) was observed within each region. After removal of bias resulting from sampling effects and population subdivision, conservativeness tests showed that the West and East Malaysia databases were conservative. This suggests that both databases can be used independently for random match probability estimation within respective regions. The reliability of the databases was further determined by independent self-assignment tests based on the likelihood of each individual's multilocus genotype occurring in each identified population, genetic cluster and region with an average percentage of correctly assigned individuals of 54.80%, 99.60% and 100% respectively. Thus, after appropriate validation, the genetic identification databases developed for G. bancanus in this study could support forensic applications and help safeguard this valuable species into the future.

Predicting dispersal of auto-gyrating fruit in tropical trees: a case study from the Dipterocarpaceae.

Seed dispersal governs the distribution of plant propagules in the landscape and hence forms the template on which density-dependent processes act. Dispersal is therefore a vital component of many species coexistence and forest dynamics models and is of applied value in understanding forest regeneration. Research on the processes that facilitate forest regeneration and restoration is given further weight in the context of widespread loss and degradation of tropical forests, and provides impetus to improve estimates of seed dispersal for tropical forest trees. South-East Asian lowland rainforests, which have been subject to severe degradation, are dominated by trees of the Dipterocarpaceae family which constitute over 40% of forest biomass. Dipterocarp dispersal is generally considered to be poor given their large, gyration-dispersed fruits. However, there is wide variability in fruit size and morphology which we hypothesize mechanistically underpins dispersal potential through the lift provided to seeds mediated by the wings. We explored experimentally how the ratio of fruit wing area to mass ("inverse wing loading," IWL) explains variation in seed dispersal kernels among 13 dipterocarp species by releasing fruit from a canopy tower. Horizontal seed dispersal distances increased with IWL, especially at high wind speeds. Seed dispersal of all species was predominantly local, with 90% of seed dispersing <10 m, although maximum dispersal distances varied widely among species. We present a generic seed dispersal model for dipterocarps based on attributes of seed morphology and provide modeled seed dispersal kernels for all dipterocarp species with IWLs of 1-50, representing 75% of species in Borneo.

Ecological implications of a flower size/number trade-off in tropical forest trees.

BACKGROUND: In angiosperms, flower size commonly scales negatively with number. The ecological consequences of this trade-off for tropical trees remain poorly resolved, despite their potential importance for tropical forest conservation. We investigated the flower size number trade-off and its implications for fecundity in a sample of tree species from the Dipterocarpaceae on Borneo. METHODOLOGY/PRINCIPAL FINDINGS: We combined experimental exclusion of pollinators in 11 species, with direct and indirect estimates of contemporary pollen dispersal in two study species and published estimates of pollen dispersal in a further three species to explore the relationship between flower size, pollinator size and mean pollen dispersal distance. Maximum flower production was two orders of magnitude greater in small-flowered than large-flowered species of Dipterocarpaceae. In contrast, fruit production was unrelated to flower size and did not differ significantly among species. Small-flowered species had both smaller-sized pollinators and lower mean pollination success than large-flowered species. Average pollen dispersal distances were lower and frequency of mating between related individuals was higher in a smaller-flowered species than a larger-flowered confamilial. Our synthesis of pollen dispersal estimates across five species of dipterocarp suggests that pollen dispersal scales positively with flower size. CONCLUSIONS AND THEIR SIGNIFICANCE: Trade-offs embedded in the relationship between flower size and pollination success contribute to a reduction in the variance of fecundity among species. It is therefore plausible that these processes could delay competitive exclusion and contribute to maintenance of species coexistence in this ecologically and economically important family of tropical trees. These results have practical implications for tree species conservation and restoration. Seed collection from small-flowered species may be especially vulnerable to cryptic genetic erosion. Our findings also highlight the potential for differential vulnerability of tropical tree species to the deleterious consequences of forest fragmentation.