Hope Hollocher

INCIPIENT SPECIATION BY SEXUAL ISOLATION IN DROSOPHILA MELANOGASTER: VARIATION IN MATING PREFERENCE AND CORRELATION BETWEEN SEXES

Genetic divergence for characters pertaining to reproductive isolation is of considerable interest in evolutionary biology. Since most studies concentrate on sibling species (for recent reviews, see Wu et al. 1996), we would like to know how much genetic variation exists between populations that are at an incipient stage of speciation. To answer this question, we have begun measuring variations in mating preference among natural isolates of Drosophila melanogaster, represented by the cosmopolitan and Zimbabwe sexual races. We quantify the variation in mating preference and success in both sexes by using a multiple‐choice design and an index that is suited to cases of strong asymmetry in mate choice. Different designs and indices for measuring sexual isolation are also discussed. These sexual traits are entirely genetically determined. Surveying four populations in southern Africa and additional cosmopolitan lines, we observe extensive genetic variation in sexual characters as well as strong correlation between sexes. The populations are highly differentiated and represent various stages of evolution between the African and the cosmopolitan type of sexual behaviors. The genetic variation and correlation for these sexual characters coupled with their geographical pattern have interesting implications for models of speciation by sexual selection.

The anthropogenic environment lessens the intensity and prevalence of gastrointestinal parasites in Balinese long-tailed macaques (Macaca fascicularis)

The distribution of wildlife parasites in a landscape is intimately tied to the spatial distribution of hosts. In parasite species, including many gastrointestinal parasites, with obligate or common environmental life stages, the dynamics of the parasite can also be strongly affected by geophysical components of the environment. This is especially salient in host species, for example humans and macaques, which thrive across a wide variety of habitat types and quality and so are exposed to a wealth of environmentally resilient parasites. Here, we examine the effect of environmental and anthropogenic components of the landscape on the prevalence, intensity, and species diversity of gastrointestinal parasites across a metapopulation of long-tailed macaques on the island of Bali, Indonesia. Using principal-components analysis, we identified significant interaction effects between specific environmental and anthropogenic components of the landscape, parsing the Balinese landscape into anthropogenic (PC1), mixed environment (PC2), and non-anthropogenic (PC3) components. Further, we determined that the anthropogenic environment can mitigate the prevalence and intensity of specific gut parasites and the intensity of the overall community of gut parasites, but that non-anthropogenically driven landscape components have no significant effect in increasing or reducing the intensity or prevalence of the community of gut parasites in Balinese macaques.

RECENT RADIATION OF ENDEMIC CARIBBEAN DROSOPHILA OF THE DUNNI SUBGROUP INFERRED FROM MULTILOCUS DNA SEQUENCE VARIATION

Abstract Studies of island endemism provide a unique opportunity to elucidate fundamental mechanisms of speciation. Here we examine intra‐ and interspecific DNA sequence variation at four unlinked genetic loci among populations of the Drosophila dunni subgroup to provide a detailed genealogical portrait of the process of speciation among these island endemic species. Our data indicate two major rounds of diversification that have shaped the D. dunni subgroup. The first occurred 1.6–2.6 million years ago and separated three major lineages, one in Puerto Rico and the Virgin Islands, a second in the northern Lesser Antilles and Barbados, and a third in St. Vincent and Grenada. A second round of diversification occurred in the last 96,000 years in the northern Lesser Antilles and Barbados. The four distinct species that resulted from this recent round of diversification maintain relatively high amounts of genetic variation, similar to that of a closely related mainland species, and share extensive ancestral polymorphism. These data suggest a minimal role for population bottlenecks linked to founder events in the history of the D. dunni subgroup. Further, the recent divergence of these island populations highlights the extremely rapid development of reproductive isolation and distinct patterns of abdominal pigmentation that has occurred in these species.

Phylogenetic analysis of the Cardini group of Drosophila with respect to changes in pigmentation.

Abstract Phenotypic variability is the engine that drives future diversification with the expectation that polymorphic ancestors give rise to descendants harboring a subset of the ancestral variation. Here we examine evolutionary transitions from polymorphism to monomorphism in a visually striking New World radiation of fruit flies, the Drosophila cardini group. This group is distributed across the Americas and the Caribbean islands and exhibits a wide spectrum of abdominal pigmentation variation. Specifically, the D. dunni subgroup consists of Caribbean island endemics, each of which is monomorphic for its pigmentation pattern, with an interspecific cline of pigmentation across the islands. The D. cardini subgroup consists of American continental species with wide-ranging distributions and intraspecifically variable abdominal pigmentation. We determined the phylogeny of 18 species and subspecies using three nuclear and three mitochondrial regions analyzed with maximum parsimony, maximum likelihood, and Bayesian methods. The topology produced from a combined dataset exhibited high support values at all nodes, and differed from earlier phylogenetic hypotheses based on polytene chromosome inversion patterns and isozyme data. We find that the D. dunni subgroup species, with the exception of D. belladunni, are derived from a single source not of direct South American origin and their dispersal across the islands of the Caribbean does not follow a simple stepping-stone model. Morphological changes in pigmentation across the island species are incongruent with the colonization history of the group indicating that natural selection may have played a role in the determination of this character. Finally, we demonstrate that monomorphic species have arisen independently from polymorphic ancestors two to three times.

Pests, Pestilence, and People: The Long-Tailed Macaque and Its Role in the Cultural Complexities of Bali

Bali’s unique religious tradition established the foundations of a system of island-wide rice agriculture that is organized around interconnected water temples, known as subaks (Lansing 2007). This temple-oriented rice agricultural system was well established at the time of the Dutch Colonization of Indonesia, approximately 500 years ago, and has remained relatively stable since that time with subaks and traditional rice agriculture practices enjoying renewed success within the last 30 years since Indonesia’s Green Revolution (Wheatley 1999; Lansing 2007). Historically, the island’s temples have effectively governed and coordinated the timing of planting, irrigating, and harvesting rice, preventing water shortages and disease outbreaks in doing so. As the site for religious, agricultural, and cultural events, the temple system acts as the cohesive and organizing power for whole villages. It is this interwoven framework of temples, rice fields, villages, and associated forest patches that forms the complex cultural and physical landscape in which Balinese long-tailed macaques (Macaca fascicularis) exist (Fuentes et al. 2005).

A test of agent-based models as a tool for predicting patterns of pathogen transmission in complex landscapes

BackgroundLandscape complexity can mitigate or facilitate host dispersal, influencing patterns of pathogen transmission. Spatial transmission of pathogens through landscapes, therefore, presents an important but not fully elucidated aspect of transmission dynamics. Using an agent-based model (LiNK) that incorporates GIS data, we examined the effects of landscape information on the spatial patterns of host movement and pathogen transmission in a system of long-tailed macaques and their gut parasites. We first examined the role of the landscape to identify any individual or additive effects on host movement. We then compared modeled dispersal distance to patterns of actual macaque gene flow to both confirm our model’s predictions and to understand the role of individual land uses on dispersal. Finally, we compared the rate and the spread of two gastrointestinal parasites, Entamoeba histolytica and E. dispar, to understand how landscape complexity influences spatial patterns of pathogen transmission.ResultsLiNK captured emergent properties of the landscape, finding that interaction effects between landscape layers could mitigate the rate of infection in a non-additive way. We also found that the inclusion of landscape information facilitated an accurate prediction of macaque dispersal patterns across a complex landscape, as confirmed by Mantel tests comparing genetic and simulated dispersed distances. Finally, we demonstrated that landscape heterogeneity proved a significant barrier for a highly virulent pathogen, limiting the dispersal ability of hosts and thus its own transmission into distant populations.ConclusionsLandscape complexity plays a significant role in determining the path of host dispersal and patterns of pathogen transmission. Incorporating landscape heterogeneity and host behavior into disease management decisions can be important in targeting response efforts, identifying cryptic transmission opportunities, and reducing or understanding potential for unintended ecological and evolutionary consequences. The inclusion of these data into models of pathogen transmission patterns improves our understanding of these dynamics, ultimately proving beneficial for sound public health policy.

Characterization and isolation of novel microsatellites from the Drosophila dunni subgroup

We have isolated and characterized 77 novel microsatellites from two species, Drosophila dunni and Drosophila nigrodunni, which are closely related Caribbean-island endemics from the Drosophila cardini species group. These species are very distantly related to all other Drosophila from which microsatellites have previously been characterized. We find that the average length of microsatellites isolated in these species is quite small, with an overall mean length of 9.8 repeat units for dinucleotide microsatellites in the two study species. The nucleotide composition of dinucleotides differs between the two species: D. nigrodunni has a predominance of (AC/GT)n repeats, whereas D. dunni has equal numbers of (AC/GT)n and (AG/CT)n repeats. Tri- and tetranucleotide repeats are not abundant in either species. We assayed the variability of eight microsatellites in a closely related third species, Drosophila arawakana, using wild-caught individuals from the island of Guadeloupe. We found the microsatellites to be extremely variable in this population, with observed heterozygosities ranging from 0.541 to 0.889. DNA amplification trials suggest that these eight microsatellites are widely conserved across the D. cardini group, with five of the eight producing amplification products in every species tested. However, the loci are very poorly conserved over greater phylogenetic distances. DNA amplification of the microsatellite loci was unreliable in members of the closely related Drosophila quinaria, Drosophila calloptera, Drosophila guarani and Drosophila tripunctata species groups. Furthermore, these microsatellites could not be detected in the genome of Drosophila melanogaster, despite the conservation of microsatellite flanking regions at some loci. These data indicate that Drosophila microsatellite loci are quite short lived over evolutionary timescales relative to many other taxa.

Human behavior and opportunities for parasite transmission in communities surrounding long-tailed macaque populations in Bali, Indonesia

Spatial overlap and shared resources between humans and wildlife can exacerbate parasite transmission dynamics. In Bali, Indonesia, an agricultural‐religious temple system provides sanctuaries for long‐tailed macaques (Macaca fascicularis), concentrating them in areas in close proximity to humans. In this study, we interviewed individuals in communities surrounding 13 macaque populations about their willingness to participate in behaviors that would put them at risk of exposure to gastrointestinal parasites to understand if age, education level, or occupation are significant determinants of exposure behaviors. These exposure risk behaviors and attitudes include fear of macaques, direct contact with macaques, owning pet macaques, hunting and eating macaques, and overlapping water uses. We find that willingness to participate in exposure risk behaviors are correlated with an individuals occupation, age, and/or education level. We also found that because the actual risk of infection varies across populations, activities such as direct macaque contact and pet ownership, could be putting individuals at real risk in certain contexts. Thus, we show that human demographics and social structure can influence willingness to participate in behaviors putting them at increased risk for exposure to parasites. Am. J. Primatol. 76:159–167, 2014.

Comparative community-level associations of helminth infections and microparasite shedding in wild long-tailed macaques in Bali, Indonesia

Helminthes have the capacity to modulate host immunity, leading to positive interactions with coinfecting microparasites. This phenomenon has been primarily studied during coinfections with a narrow range of geo-helminthes and intracellular microparasites in human populations or under laboratory conditions. Far less is known regarding differences in coinfection dynamics between helminth types, the range of microparasites that might be affected or the overall community-level effects of helminth infections on microparasites in wild systems. Here, we analysed the presence/absence and abundance patterns of enteric parasites in long-tailed macaques (Macaca fascicularis) on the island of Bali, Indonesia, to assess whether naturally occurring helminth infections were associated with increased shedding of the most common intracellular (Cryptosporidium spp., Isospora spp.) and extracellular (Entamoeba spp., Giardia spp.) microparasites. We also comparatively assessed the statistical correlations of different helminth taxa with microparasite shedding to determine if there were consistent relationships between the specific helminth taxa and microparasites. Helminth infections were associated with increased shedding of both intracellular and extracellular microparasites. Platyhelminthes repeatedly displayed strong positive correlations with several microparasites; while nematodes did not. Our results indicate that helminthes can influence microparasite community shedding dynamics under wild conditions, but that trends may be driven by a narrow range of helminthes.

Bayesian inference reveals ancient origin of simian foamy virus in orangutans

Simian foamy viruses (SFVs) infect most nonhuman primate species and appears to co-evolve with its hosts. This co-evolutionary signal is particularly strong among great apes, including orangutans (genus Pongo). Previous studies have identified three distinct orangutan SFV clades. The first of these three clades is composed of SFV from P. abelii from Sumatra, the second consists of SFV from P. pygmaeus from Borneo, while the third clade is mixed, comprising an SFV strain found in both species of orangutan. The existence of the mixed clade has been attributed to an expansion of P. pygmaeus into Sumatra following the Mount Toba super-volcanic eruption about 73,000years ago. Divergence dating, however, has yet to be performed to establish a temporal association with the Toba eruption. Here, we use a Bayesian framework and a relaxed molecular clock model with fossil calibrations to test the Toba hypothesis and to gain a more complete understanding of the evolutionary history of orangutan SFV. As with previous studies, our results show a similar three-clade orangutan SFV phylogeny, along with strong statistical support for SFV-host co-evolution in orangutans. Using Bayesian inference, we date the origin of orangutan SFV to >4.7 million years ago (mya), while the mixed species clade dates to approximately 1.7mya, >1.6 million years older than the Toba super-eruption. These results, combined with fossil and paleogeographic evidence, suggest that the origin of SFV in Sumatran and Bornean orangutans, including the mixed species clade, likely occurred on the mainland of Indo-China during the Late Pliocene and Calabrian stage of the Pleistocene, respectively.