Kathryn Jane Jeffery

Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers

Population bottlenecks are often invoked to explain low levels of genetic variation in natural populations, yet few studies have documented the direct genetic consequences of known bottlenecks in the wild. Empirical studies of natural population bottlenecks are therefore needed, because key assumptions of theoretical and laboratory studies of bottlenecks may not hold in the wild. Here we present microsatellite data from a severe bottleneck (95% mortality) in an insular population of song sparrows (Melospiza melodia). The major findings of our study are as follows: (i) The bottleneck reduced heterozygosity and allelic diversity nearly to neutral expectations, despite non–random survival of birds with respect to inbreeding and wing length. (ii) All measures of genetic diversity regained pre–bottleneck levels within two to three years of the crash. This rapid recovery was due to low levels of immigration. (iii) The rapid recovery occurred despite a coincident, strong increase in average inbreeding. These results show that immigration at levels that are hard to measure in most field studies can lead to qualitatively very different genetic outcomes from those expected from mutations only. We suggest that future theoretical and empirical work on bottlenecks and metapopulations should address the impact of immigration.

The role of Pleistocene refugia and rivers in shaping gorilla genetic diversity in central Africa

The role of Pleistocene forest refugia and rivers in the evolutionary diversification of tropical biota has been the subject of considerable debate. A range-wide analysis of gorilla mitochondrial and nuclear variation was used to test the potential role of both refugia and rivers in shaping genetic diversity in current populations. Results reveal strong patterns of regional differentiation that are consistent with refugial hypotheses for central Africa. Four major mitochondrial haplogroups are evident with the greatest divergence between eastern (A, B) and western (C, D) gorillas. Coalescent simulations reject a model of recent east–west separation during the last glacial maximum but are consistent with a divergence time within the Pleistocene. Microsatellite data also support a similar regional pattern of population genetic structure. Signatures of demographic expansion were detected in eastern lowland (B) and Gabon/Congo (D3) mitochondrial haplogroups and are consistent with a history of postglacial expansion from formerly isolated refugia. Although most mitochondrial haplogroups are regionally defined, limited admixture is evident between neighboring haplogroups. Mantel tests reveal a significant isolation-by-distance effect among western lowland gorilla populations. However, mitochondrial genetic distances also correlate with the distance required to circumnavigate intervening rivers, indicating a possible role for rivers in partitioning gorilla genetic diversity. Comparative data are needed to evaluate the importance of both mechanisms of vicariance in other African rainforest taxa.

Mitochondrial DNA phylogeography of western lowland gorillas (Gorilla gorilla gorilla)

The geographical distribution of genetic variation within western lowland gorillas (Gorilla gorilla gorilla) was examined to clarify the population genetic structure and recent evolutionary history of this group. DNA was amplified from shed hair collected from sites across the range of the three traditionally recognized gorilla subspecies: western lowland (G. g. gorilla), eastern lowland (G. g. graueri) and mountain (G. g. beringei) gorillas. Nucleotide sequence variation was examined in the first hypervariable domain of the mitochondrial control region and was much higher in western lowland gorillas than in either of the other two subspecies. In addition to recapitulating the major evolutionary split between eastern and western lowland gorillas, phylogenetic analysis indicates a phylogeographical division within western lowland gorillas, one haplogroup comprising gorilla populations from eastern Nigeria through to southeast Cameroon and a second comprising all other western lowland gorillas. Within this second haplogroup, haplotypes appear to be partitioned geographically into three subgroups: (i) Equatorial Guinea, (ii) Central African Republic, and (iii) Gabon and adjacent Congo. There is also evidence of limited haplotype admixture in northeastern Gabon and southeast Cameroon. The phylogeographical patterns are broadly consistent with those predicted by current Pleistocene refuge hypotheses for the region and suggest that historical events have played an important role in shaping the population structure of this subspecies.

Novel Adenoviruses in Wild Primates: a High Level of Genetic Diversity and Evidence of Zoonotic Transmissions

ABSTRACT Adenoviruses (AdVs) broadly infect vertebrate hosts, including a variety of nonhuman primates (NHPs). In the present study, we identified AdVs in NHPs living in their natural habitats, and through the combination of phylogenetic analyses and information on the habitats and epidemiological settings, we detected possible horizontal transmission events between NHPs and humans. Wild NHPs were analyzed with a pan-primate AdV-specific PCR using a degenerate nested primer set that targets the highly conserved adenovirus DNA polymerase gene. A plethora of novel AdV sequences were identified, representing at least 45 distinct AdVs. From the AdV-positive individuals, 29 nearly complete hexon genes were amplified and, based on phylogenetic analysis, tentatively allocated to all known human AdV species (Human adenovirus A to Human adenovirus G [HAdV-A to -G]) as well as to the only simian AdV species (Simian adenovirus A [SAdV-A]). Interestingly, five of the AdVs detected in great apes grouped into the HAdV-A, HAdV-D, HAdV-F, or SAdV-A clade. Furthermore, we report the first detection of AdVs in New World monkeys, clustering at the base of the primate AdV evolutionary tree. Most notably, six chimpanzee AdVs of species HAdV-A to HAdV-F revealed a remarkably close relationship to human AdVs, possibly indicating recent interspecies transmission events.

Chimpanzee accumulative stone throwing

The study of the archaeological remains of fossil hominins must rely on reconstructions to elucidate the behaviour that may have resulted in particular stone tools and their accumulation. Comparatively, stone tool use among living primates has illuminated behaviours that are also amenable to archaeological examination, permitting direct observations of the behaviour leading to artefacts and their assemblages to be incorporated. Here, we describe newly discovered stone tool-use behaviour and stone accumulation sites in wild chimpanzees reminiscent of human cairns. In addition to data from 17 mid- to long-term chimpanzee research sites, we sampled a further 34 Pan troglodytes communities. We found four populations in West Africa where chimpanzees habitually bang and throw rocks against trees, or toss them into tree cavities, resulting in conspicuous stone accumulations at these sites. This represents the first record of repeated observations of individual chimpanzees exhibiting stone tool use for a purpose other than extractive foraging at what appear to be targeted trees. The ritualized behavioural display and collection of artefacts at particular locations observed in chimpanzee accumulative stone throwing may have implications for the inferences that can be drawn from archaeological stone assemblages and the origins of ritual sites.

African Savanna-Forest Boundary Dynamics: A 20-Year Study

Recent studies show widespread encroachment of forest into savannas with important consequences for the global carbon cycle and land-atmosphere interactions. However, little research has focused on in situ measurements of the successional sequence of savanna to forest in Africa. Using long-term inventory plots we quantify changes in vegetation structure, above-ground biomass (AGB) and biodiversity of trees ≥10 cm diameter over 20 years for five vegetation types: savanna; colonising forest (F1), monodominant Okoume forest (F2); young Marantaceae forest (F3); and mixed Marantaceae forest (F4) in Lopé National Park, central Gabon, plus novel 3D terrestrial laser scanning (TLS) measurements to assess forest structure differences. Over 20 years no plot changed to a new stage in the putative succession, but F1 forests strongly moved towards the structure, AGB and diversity of F2 forests. Overall, savanna plots showed no detectable change in structure, AGB or diversity using this method, with zero trees ≥10 cm diameter in 1993 and 2013. F1 and F2 forests increased in AGB, mainly as a result of adding recruited stems (F1) and increased Basal Area (F2), whereas F3 and F4 forests did not change substantially in structure, AGB or diversity. Critically, the stability of the F3 stage implies that this stage may be maintained for long periods. Soil carbon was low, and did not show a successional gradient as for AGB and diversity. TLS vertical plant profiles showed distinctive differences amongst the vegetation types, indicating that this technique can improve ecological understanding. We highlight two points: (i) as forest colonises, changes in biodiversity are much slower than changes in forest structure or AGB; and (ii) all forest types store substantial quantities of carbon. Multi-decadal monitoring is likely to be required to assess the speed of transition between vegetation types.

Fine-Scale Genetic Structure and Cryptic Associations Reveal Evidence of Kin-Based Sociality in the African Forest Elephant

Spatial patterns of relatedness within animal populations are important in the evolution of mating and social systems, and have the potential to reveal information on species that are difficult to observe in the wild. This study examines the fine-scale genetic structure and connectivity of groups within African forest elephants, Loxodonta cyclotis, which are often difficult to observe due to forest habitat. We tested the hypothesis that genetic similarity will decline with increasing geographic distance, as we expect kin to be in closer proximity, using spatial autocorrelation analyses and Tau Kr tests. Associations between individuals were investigated through a non-invasive genetic capture-recapture approach using network models, and were predicted to be more extensive than the small groups found in observational studies, similar to fission-fusion sociality found in African savanna (Loxodonta africana) and Asian (Elephas maximus) species. Dung samples were collected in Lopé National Park, Gabon in 2008 and 2010 and genotyped at 10 microsatellite loci, genetically sexed, and sequenced at the mitochondrial DNA control region. We conducted analyses on samples collected at three different temporal scales: a day, within six-day sampling sessions, and within each year. Spatial autocorrelation and Tau Kr tests revealed genetic structure, but results were weak and inconsistent between sampling sessions. Positive spatial autocorrelation was found in distance classes of 0–5 km, and was strongest for the single day session. Despite weak genetic structure, individuals within groups were significantly more related to each other than to individuals between groups. Social networks revealed some components to have large, extensive groups of up to 22 individuals, and most groups were composed of individuals of the same matriline. Although fine-scale population genetic structure was weak, forest elephants are typically found in groups consisting of kin and based on matrilines, with some individuals having more associates than observed from group sizes alone.

Field and Laboratory Methods in Primatology: Collection, storage and analysis of non-invasive genetic material in primate biology

WHY NON-INVASIVE? Non-invasive genetic analysis using new, high-precision molecular tools has been an extremely important recent development in primatology, with the promise of pioneering studies in the early–mid 1990s (see, for example, Morin et al ., 1994) now being realized at the level of large-scale population studies over broad spatial scales (see, for example, Constable et al ., 2001; Anthony et al ., 2007b). However, it remains technically demanding, time-consuming, expensive and prone to error. Here, we introduce the applications of non-invasive genetics in primatology, then cover protocols for the most common non-invasive sample types, including faeces, urine and hair, outlining the limitations, pitfalls, and methodologies required. We also describe storage protocols for other possible sources of DNA (deoxyribonucleic acid), including blood and tissue biopsy samples for occasions when animals are captured and handled (Chapters 7 and 8). APPLICATIONS Molecular phylogenetic studies continue to add to our knowledge of primate diversity, evolution and hence adaptation (see, for example, Burrell et al ., 2009). Phylogenetic analysis can also be used below the species level to study the underlying biogeographical factors that have contributed to the diversity present in primate populations today. This approach has been used to highlight new, evolutionarily distinct populations within well-studied species and to pinpoint potentially important geographical barriers that may delimit genetic divergences across the range of species (see, for example, Gonder et al ., 1997).

Fourier analysis to detect phenological cycles using long‐term tropical field data and simulations

1.Changes in phenology are an inevitable result of climate change, and will have wide-reaching impacts on species, ecosystems, human society and even feedback onto climate. Accurate understanding of phenology is important to adapt to and mitigate such changes. However, analysis of phenology globally has been constrained by lack of data, dependence on geographically limited, non-circular indicators and lack of power in statistical analyses. 2.To address these challenges, especially for the study of tropical phenology, we developed a flexible and robust analytical approach - using Fourier analysis with confidence intervals - to objectively and quantitatively describe long-term observational phenology data even when data may be noisy. We then tested the power of this approach to detect regular cycles under different scenarios of data noise and length using both simulated and field data. 3.We use Fourier analysis to quantify flowering phenology from newly available data for 856 individual plants of 70 species observed monthly since 1986 at Lope National Park, Gabon. After applying a confidence test, we find that 59% of the individuals have regular flowering cycles, and 88% species flower annually. We find time series length to be a significant predictor of the likelihood of confidently detecting a regular cycle from the data. Using simulated data we find that cycle regularity has a greater impact on detecting phenology than event detectability. Power analysis of the Lope field data shows that at least six years of data are needed for confident detection of the least noisy species, but this varies and is often greater than 20 years for the most noisy species. 4.There are now a number of large phenology datasets from the tropics, from which insights into current regional and global changes may be gained, if flexible and quantitative analytical approaches are used. However consistent long-term data collection is costly and requires much effort. We provide support for the importance of such research and give suggestions as to how to avoid erroneous interpretation of shorter length datasets and maximize returns from long-term observational studies. This article is protected by copyright. All rights reserved.

A universal microsatellite multiplex kit for genetic analysis of great apes.

DNA profiling with microsatellite markers is a commonly used genetic method of studying the great apes. An efficient method of generating the genetic data is amplification of multiple microsatellites in a single PCR reaction. Here we describe a PCR multiplex in which 9 genetic markers can be amplified simultaneously, thereby saving time, expenses and DNA. This marker system can discriminate between all the great ape species except bonobos and chimpanzees. Furthermore, the cumulative probability of identity values were low for all 4 species tested.