Erik P. Willems

Effects of Pleistocene glaciations and rivers on the population structure of Bornean orangutans (Pongo pygmaeus)

Sundaland, a tropical hotspot of biodiversity comprising Borneo and Sumatra among other islands, the Malay Peninsula, and a shallow sea, has been subject to dramatic environmental processes. Thus, it presents an ideal opportunity to investigate the role of environmental mechanisms in shaping species distribution and diversity. We investigated the population structure and underlying mechanisms of an insular endemic, the Bornean orangutan (Pongo pygmaeus). Phylogenetic reconstructions based on mtDNA sequences from 211 wild orangutans covering the entire range of the species indicate an unexpectedly recent common ancestor of Bornean orangutans 176 ka (95% highest posterior density, 72–322 ka), pointing to a Pleistocene refugium. High mtDNA differentiation among populations and rare haplotype sharing is consistent with a pattern of strong female philopatry. This is corroborated by isolation by distance tests, which show a significant correlation between mtDNA divergence and distance and a strong effect of rivers as barriers for female movement. Both frequency-based and Bayesian clustering analyses using as many as 25 nuclear microsatellite loci revealed a significant separation among all populations, as well as a small degree of male-mediated gene flow. This study highlights the unique effects of environmental and biological features on the evolutionary history of Bornean orangutans, a highly endangered species particularly vulnerable to future climate and anthropogenic change as an insular endemic.

Sex-Biased Dispersal and Volcanic Activities Shaped Phylogeographic Patterns of Extant Orangutans (genus: Pongo)

The Southeast Asian Sunda archipelago harbors a rich biodiversity with a substantial proportion of endemic species. The evolutionary history of these species has been drastically influenced by environmental forces, such as fluctuating sea levels, climatic changes, and severe volcanic activities. Orangutans (genus: Pongo), the only Asian great apes, are well suited to study the relative impact of these forces due to their well-documented behavioral ecology, strict habitat requirements, and exceptionally slow life history. We investigated the phylogeographic patterns and evolutionary history of orangutans in the light of the complex geological and climatic history of the Sunda archipelago. Our study is based on the most extensive genetic sampling to date, covering the entire range of extant orangutan populations. Using data from three mitochondrial DNA (mtDNA) genes from 112 wild orangutans, we show that Sumatran orangutans, Pongo abelii, are paraphyletic with respect to Bornean orangutans (P. pygmaeus), the only other currently recognized species within this genus. The deepest split in the mtDNA phylogeny of orangutans occurs across the Toba caldera in northern Sumatra and, not as expected, between both islands. Until the recent past, the Toba region has experienced extensive volcanic activity, which has shaped the current phylogeographic patterns. Like their Bornean counterparts, Sumatran orangutans exhibit a strong, yet previously undocumented structuring into four geographical clusters. However, with 3.50 Ma, the Sumatran haplotypes have a much older coalescence than their Bornean counterparts (178 kya). In sharp contrast to the mtDNA data, 18 Y-chromosomal polymorphisms show a much more recent coalescence within Sumatra compared with Borneo. Moreover, the deep geographic structure evident in mtDNA is not reflected in the male population history, strongly suggesting male-biased dispersal. We conclude that volcanic activities have played an important role in the evolutionary history of orangutans and potentially of many other forest-dwelling Sundaland species. Furthermore, we demonstrate that a strong sex bias in dispersal can lead to conflicting patterns in uniparentally inherited markers even at a genus-wide scale, highlighting the need for a combined usage of maternally and paternally inherited marker systems in phylogenetic studies.

LARGE BRAINS BUFFER ENERGETIC EFFECTS OF SEASONAL HABITATS IN CATARRHINE PRIMATES

Ecological factors have been shown to be important for brain size evolution. In this comparative study among catarrhine primates, we examine two different ways in which seasonality may be related to brain size. First, seasonality may impose energetic constraints on the brain because it forces animals to deal with periods of food scarcity (Expensive Brain hypothesis). Second, seasonality may act as a selective pressure to increase brain size, as behavioral flexibility helps to overcome periods of food scarcity (Cognitive Buffer hypothesis). Controlling for phylogeny, we found a strong negative relationship between brain size (relative to body mass) and the degree of experienced seasonality, as estimated by the variation in net energy intake. However, we also found a significant positive relationship between relative brain size and the effect of so‐called cognitive buffering, proxied by the difference between environmental seasonality and the seasonality in net energy intake actually experienced by the animals. These results show that both energetic constraints of seasonal habitats as well as cognitive buffering affect brain size evolution, leaving environmental seasonality uncorrelated to brain size. With this study we show the importance of simultaneously considering both costs and benefits in models of brain size evolution.

Understanding the Impacts of Land-Use Policies on a Threatened Species: Is There a Future for the Bornean Orang-utan?

The geographic distribution of Bornean orang-utans and its overlap with existing land-use categories (protected areas, logging and plantation concessions) is a necessary foundation to prioritize conservation planning. Based on an extensive orang-utan survey dataset and a number of environmental variables, we modelled an orang-utan distribution map. The modelled orang-utan distribution map covers 155,106 km2 (21% of Borneos landmass) and reveals four distinct distribution areas. The most important environmental predictors are annual rainfall and land cover. The overlap of the orang-utan distribution with land-use categories reveals that only 22% of the distribution lies in protected areas, but that 29% lies in natural forest concessions. A further 19% and 6% occurs in largely undeveloped oil palm and tree plantation concessions, respectively. The remaining 24% of the orang-utan distribution range occurs outside of protected areas and outside of concessions. An estimated 49% of the orang-utan distribution will be lost if all forest outside of protected areas and logging concessions is lost. To avoid this potential decline plantation development in orang-utan habitats must be halted because it infringes on national laws of species protection. Further growth of the plantation sector should be achieved through increasing yields in existing plantations and expansion of new plantations into areas that have already been deforested. To reach this goal a large scale island-wide land-use masterplan is needed that clarifies which possible land uses and managements are allowed in the landscape and provides new standardized strategic conservation policies. Such a process should make much better use of non-market values of ecosystem services of forests such as water provision, flood control, carbon sequestration, and sources of livelihood for rural communities. Presently land use planning is more driven by vested interests and direct and immediate economic gains, rather than by approaches that take into consideration social equity and environmental sustainability.

The collective action problem in primate territory economics

Group-living animals often do not maintain territories, but instead have highly overlapping ranges, even though in principle these are economically defendable. We investigate whether this absence of range defence reflects a collective action problem, since a territory can be considered a public good. In a comparative analysis comprising 135 primate species, we find a positive association between range overlap and group size, controlling for economic defendability and phylogenetic non-independence. We subsequently demonstrate that groups with multiple adults of both sexes suffer levels of range overlap twice as high as groups with only a single adult representative of either sex, consistent with the presence of a collective action problem. Finally, we reveal that this collective action problem can be overcome through philopatry of the larger sex. These results suggest that a social complication of group living is a stronger determinant of between-group relations among social animals than ecological factors, but also that collective defence is still achieved where the dominant sex is philopatric and effective defence is critical to reproductive success and survival. In addition, our findings support the idea that human-like warfare, defined as escalated collective territorial conflict, has an evolutionary basis reflected by cases of convergent evolution among non-human primates.

Female dispersal, inbreeding avoidance and mate choice in Thomas langurs (Presbytis thomasi)

Female social dispersal in primates differs from the general mammalian pattern of locational dispersal. Both nulliparous and parous females may disperse to another group. Several hypotheses can explain female social dispersal: reduction of predation risk, inbreeding avoidance, and offspring protection through mate choice. We tested these hypotheses with an extended data set of Thomas langurs (Presbytis thomasi) and investigated parameters of male behaviour that females may use in their dispersal decisions. Data were collected over a 12.5-year period from a wild population in Sumatra, Indonesia, allowing for some critical tests of the hypotheses. Females dispersed to a group smaller than their original one, thereby refuting the predation risk hypothesis. Maturing nulliparous females only dispersed when their father was resident. Therefore, dispersal by nulliparous females was best explained through inbreeding avoidance. Parous females transferred to young, adult males. These males provided better protection to offspring against predation and infanticide than the old, late tenure males. Therefore, females transfer to better protector males. The male behavioural cues that females use to assess male quality were unclear. Females, however, may use proxies of male age, such as group composition and acoustical characteristics of loud calls, as indicators of male quality. The results suggest that female mate choice is an important function of social dispersal by parous females. Its importance in locational dispersal remains to be investigated.

Species-specific patterns in fecal glucocorticoid and androgen levels in zoo-living orangutans (Pongo spp.).

In contrast to most primate species, including the other great apes, orangutans maintain a fission-fusion social system in the wild without being part of a stable community. In zoos, however, they are kept in permanent groups, usually consisting of one adult male and several females. In zoo orangutans, we predict higher levels of glucocorticoids and androgens in the Bornean species compared to its congener from Sumatra, due to the much more solitary lifestyle of Bornean orangutans and the apparent higher frequency of male aggression directed towards females in this species in the wild. To compare hormone levels of the two orangutan species, we validated a fecal glucocorticoid and a fecal androgen assay. Subsequently, fecal samples from a total of 73 female and 38 male orangutans housed in 29 European zoos were analyzed to investigate the effect of species, social group size, age and (for female glucocorticoid levels) reproductive state and the presence of adult males on fecal hormone metabolite concentrations. The results of linear mixed effect models indicate that both male and female Bornean orangutans show a steeper increase in glucocorticoid levels with increasing group size than Sumatran orangutans. We therefore conclude that Sumatran zoo orangutans are better able to adjust to social housing conditions than their Bornean congeners. In addition, our analyses reveal higher glucocorticoid levels in lactating females of both species compared to non-lactating and juvenile females. Concerning androgen levels in males, our analyses revealed significantly higher concentrations in Bornean than Sumatran orangutans. These differences in both glucocorticoid and androgen output between the two species of orangutan are presumably linked to ecological and behavioral differences and could possibly be attributed to phenotypic plasticity. However, given that we found interspecific differences in hormone excretion in captivity, where both species live under very similar conditions, we conclude that this variation has a genetic basis.

Quantitative Transcriptomics using Designed Primer-based Amplification

We developed a novel Designed Primer-based RNA-sequencing strategy (DP-seq) that uses a defined set of heptamer primers to amplify the majority of expressed transcripts from limiting amounts of mRNA, while preserving their relative abundance. Our strategy reproducibly yielded high levels of amplification from as low as 50 picograms of mRNA while offering a dynamic range of over five orders of magnitude in RNA concentrations. We also demonstrated the potential of DP-seq to selectively suppress the amplification of the highly expressing ribosomal transcripts by more than 70% in our sequencing library. Using lineage segregation in embryonic stem cell cultures as a model of early mammalian embryogenesis, DP-seq revealed novel sets of low abundant transcripts, some corresponding to the identity of cellular progeny before they arise, reflecting the specification of cell fate prior to actual germ layer segregation.

Parentage-based pedigree reconstruction reveals female matrilineal clusters and male-biased dispersal in nongregarious Asian great apes, the Bornean orang-utans (Pongo pygmaeus)

Philopatry and sex‐biased dispersal have a strong influence on population genetic structure, so the study of species dispersal patterns and evolutionary mechanisms shaping them are of great interest. Particularly nongregarious mammalian species present an underexplored field of study: despite their lower levels of sociality compared to group‐living species, interactions among individuals do occur, providing opportunities for cryptic kin selection. Among the least gregarious primates are orang‐utans (genus: Pongo), in which preferential associations among females have nevertheless been observed, but for which the presence of kin structures was so far unresolved because of the equivocal results of previous genetic studies. To clarify relatedness and dispersal patterns in orang‐utans, we examined the largest longitudinal set of individuals with combined genetic, spatial and behavioural data. We found that males had significantly higher mitochondrial DNA (mtDNA) variation and more unique haplotypes, thus underscoring their different maternal ancestries compared to females. Moreover, pedigree reconstruction based on 24 highly polymorphic microsatellite markers and mtDNA haplotypes demonstrated the presence of three matrilineal clusters of generally highly related females with substantially overlapping ranges. In orang‐utans and possibly other nongregarious species, comparing average biparental relatedness (r) of males and females to infer sex‐biased dispersal is extremely problematic. This is because the opportunistic sampling regime frequently employed in nongregarious species, combined with overlapping space use of distinct matrilineal clusters, leads to a strong downward bias when mtDNA lineage membership is ignored. Thus, in nongregarious species, correct inferences of dispersal can only be achieved by combining several genetic approaches with detailed spatial information.

Detecting movement patterns using Brownian bridges

In trajectory data a low sampling rate leads to high uncertainty in between sampling points, which needs to be taken into account in the analysis of such data. However, current algorithms for movement analysis ignore this uncertainty and assume linear movement between sample points. In this paper we develop a framework for movement analysis using the Brownian bridge movement model (BBMM), that is, a model that assumes random movement between sample points. Many movement patterns are composed from basic building blocks, like distance, speed or direction. We efficiently compute their distribution over space and time in the BBMM using parallel graphics hardware. We demonstrate our framework by computing patterns like encounter, avoidance/attraction, regular visits, and following. Our motivation to study the BBMM stems from the rapidly expanding research paradigm of movement ecology. To this end, we provide an interface to our framework in R, an environment widely used within the natural sciences for statistical computing and modeling, and present a study on the simultaneous movement of groups of wild and free-ranging primates.