Biodiversity and vector-borne diseases: Host dilution and vector amplification occur simultaneously for Amazonian leishmaniases.

Changes in biodiversity may impact infectious disease transmission through multiple mechanisms. We explored the impact of biodiversity changes on the transmission of Amazonian leishmaniases, a group of wild zoonoses transmitted by phlebotomine sand flies (Psychodidae), which represent an important health burden in a region where biodiversity is both rich and threatened. Using molecular analyses of sand fly pools and blood-fed dipterans, we characterized the disease system in forest sites in French Guiana undergoing different levels of human-induced disturbance. We show that the prevalence of Leishmania parasites in sand flies correlates positively with the relative abundance of mammal species known as Leishmania reservoirs. In addition, Leishmania reservoirs tend to dominate in less diverse mammal communities, in accordance with the dilution effect hypothesis. This results in a negative relationship between Leishmania prevalence and mammal diversity. On the other hand, higher mammal diversity is associated with higher sand fly density, possibly because more diverse mammal communities harbor higher biomass and more abundant feeding resources for sand flies, although more research is needed to identify the factors that shape sand fly communities. As a consequence of these antagonistic effects, decreased mammal diversity comes with an increase of parasite prevalence in sand flies, but has no detectable impact on the density of infected sand flies. These results represent additional evidence that biodiversity changes may simultaneously dilute and amplify vector-borne disease transmission through different mechanisms that need to be better understood before drawing generalities on the biodiversity-disease relationship.

Bayesian Analyses of Comparative Data with the Ornstein-Uhlenbeck Model: Potential Pitfalls.

The Ornstein-Uhlenbeck (OU) model is widely used in comparative phylogenetic analyses to study the evolution of quantitative traits. It has been applied to various purposes, including the estimation of the strength of selection or ancestral traits, inferring the existence of several selective regimes, or accounting for phylogenetic correlation in regression analyses. Most programs implementing statistical inference under the OU model have resorted to maximum-likelihood (ML) inference until the recent advent of Bayesian methods. A series of issues have been noted for ML inference using the OU model, including parameter nonidentifiability. How these problems translate to a Bayesian framework has not been studied much to date and is the focus of the present article. In particular, I aim to assess the impact of the choice of priors on parameter estimates. I show that complex interactions between parameters may cause the priors for virtually all parameters to impact inference in sometimes unexpected ways, whatever the purpose of inference. I specifically draw attention to the difficulty of setting the prior for the selection strength parameter, a task to be undertaken with much caution. I particularly address investigators who do not have precise prior information, by highlighting the fact that the effect of the prior for one parameter is often only visible through its impact on the estimate of another parameter. Finally, I propose a new parameterization of the OU model that can be helpful when prior information about the parameters is not available. [Bayesian inference; Brownian motion; Ornstein-Uhlenbeck model; phenotypic evolution; phylogenetic comparative methods; prior distribution; quantitative trait evolution.].

A road map for phylogenetic models of species trees.

The field of phylogenetics has burgeoned into a great diversity of statistical models, providing researchers with a vast amount of analytical tools for investigating the evolutionary theory. This abundance of theoretical work has the merit that many different aspects of evolution can be investigated using various types of data. However, empiricists may sometimes struggle to find the right model for their needs amid such variety. In particular, some computer programs gather the theory of many different models, published in hundreds of different papers, within the same operational framework. This makes it particularly difficult for users to obtain comprehensive information about the assumptions and structure of various models. Yet, a large part of phylogenetic models are structured in individual modules that can be linked together in the same conceptual framework, akin to some sort of phylogenetic supermodel. In this paper, we propose to browse through the network of phylogenetic models, emphasizing their modular structure, with the purpose to outline the commonalities and differences of individual models. Focusing on probabilistic models, we describe how to go from the model assumptions to the corresponding probability distributions as pedagogically as possible. To achieve this task, we resort heavily on graph theory to represent the probabilistic relationships among parameters and data, and present the models in their most elementary form (i.e. including parameters that are generally marginalized out), which simplifies the mathematics considerably. We concentrate on models designed for species trees, but evoke the link with other types of trees (e.g. gene trees).

Diversity, biogeography, and reproductive evolution in the genus Pipa (Amphibia: Anura: Pipidae).

The genus Pipa is a species-poor clade of Neotropical frogs and one of the most bizarre-looking due to many highly derived anatomical traits related to their fully aquatic lifestyle. With their African relatives, they form the Pipidae family, which has attracted much attention, especially regarding its anatomy, reproductive biology, paleontology and biogeography. However, the actual diversity and phylogenetic relationships within Pipa remain poorly understood, and thus so do their historical biogeography and the evolution of striking features, such as the absence of teeth and endotrophy in some species. Using short mtDNA sequences across the distribution of the genus, we identified 15 main lineages (Operational Taxonomic Units - OTUs). This more than doubles the number of the currently seven valid nominal species. Several closely related OTUs do not share nuDNA alleles, confirming species divergence. Time-calibrated phylogenies obtained from mitogenomes and from 10 nuclear loci provide highly similar topologies but strikingly distinct node ages for Pipa. High dN/dS ratios and the variation of substitution rates across the trees suggest a strong effect of saturation on fast evolving positions of mtDNA, producing a substantially shorter stem branch of Pipa. Focusing on the nuDNA topology, we inferred an early Neogene Amazonian origin of the diversification of Pipa, with an initial split between the Guiana-Brazilian Shields and Western Amazonia, a pattern observed in many other co-distributed groups. All the western species are edentate, suggesting a single loss in the genus. Each of these groups diversified further out of Amazonia, toward the Atlantic Forest and toward trans-Andean forests, respectively. These events are concomitant with paleogeographic changes and match patterns observed in other co-distributed taxonomic groups. The two Amazonian lineages have probably independently acquired endotrophic larval development.

Data integration methods to account for spatial niche truncation effects in regional projections of species distribution.

Many species distribution models (SDMs) are built with precise but geographically restricted presence-absence data sets (e.g., a country) where only a subset of the environmental conditions experienced by a species across its range is considered (i.e., spatial niche truncation). This type of truncation is worrisome because it can lead to incorrect predictions e.g., when projecting to future climatic conditions belonging to the species niche but unavailable in the calibration area. Data from citizen-science programs, species range maps or atlases covering the full species range can be used to capture those parts of the species' niche that are missing regionally. However, these data usually are too coarse or too biased to support regional management. Here, we aim to (1) demonstrate how varying degrees of spatial niche truncation affect SDMs projections when calibrated with climatically truncated regional data sets and (2) test the performance of different methods to harness information from larger-scale data sets presenting different spatial resolutions to solve the spatial niche truncation problem. We used simulations to compare the performance of the different methods, and applied them to a real data set to predict the future distribution of a plant species (Potentilla aurea) in Switzerland. SDMs calibrated with geographically restricted data sets expectedly provided biased predictions when projected outside the calibration area or time period. Approaches integrating information from larger-scale data sets using hierarchical data integration methods usually reduced this bias. However, their performance varied depending on the level of spatial niche truncation and how data were combined. Interestingly, while some methods (e.g., data pooling, downscaling) performed well on both simulated and real data, others (e.g., those based on a Poisson point process) performed better on real data, indicating a dependency of model performance on the simulation process (e.g., shape of simulated response curves). Based on our results, we recommend to use different data integration methods and, whenever possible, to make a choice depending on model performance. In any case, an ensemble modeling approach can be used to account for uncertainty in how niche truncation is accounted for and identify areas where similarities/dissimilarities exist across methods.

Candidate Gene Analysis Suggests Untapped Genetic Complexity in Melanin-Based Pigmentation in Birds.

Studies on melanin-based color variation in a context of natural selection have provided a wealth of information on the link between phenotypic and genetic variation. Here, we evaluated associations between melanic plumage patterns and genetic polymorphism in the Réunion grey white-eye (Zosterops borbonicus), a species in which mutations on MC1R do not seem to play any role in explaining melanic variation. This species exhibits 5 plumage color variants that can be grouped into 3 color forms which occupy discrete geographic regions in the lowlands of Réunion, and a fourth high-elevation form which comprises 2 color morphs (grey and brown) and represents a true color polymorphism. We conducted a comprehensive survey of sequence variation in 96 individuals at a series of 7 candidate genes other than MC1R that have been previously shown to influence melanin-based color patterns in vertebrates, including genes that have rarely been studied in a wild bird species before: POMC, Agouti, TYR, TYRP1, DCT, Corin, and SLC24A5 Of these 7 genes, 2 (Corin and TYRP1) displayed an interesting shift in allele frequencies between lowland and highland forms and a departure from mutation-drift equilibrium consistent with balancing selection in the polymorphic highland form only. Sequence variation at Agouti, a gene frequently involved in melanin-based pigmentation patterning, was not associated with color forms or morphs. Thus, we suggest that functionally important changes in loci other than those classically studied are involved in the color polymorphism exhibited by the Réunion grey white-eye and possibly many other nonmodel species.

Islands as model systems in ecology and evolution: prospects fifty years after MacArthur-Wilson.

The study of islands as model systems has played an important role in the development of evolutionary and ecological theory. The 50th anniversary of MacArthur and Wilson's (December 1963) article, 'An equilibrium theory of insular zoogeography', was a recent milestone for this theme. Since 1963, island systems have provided new insights into the formation of ecological communities. Here, building on such developments, we highlight prospects for research on islands to improve our understanding of the ecology and evolution of communities in general. Throughout, we emphasise how attributes of islands combine to provide unusual research opportunities, the implications of which stretch far beyond islands. Molecular tools and increasing data acquisition now permit re-assessment of some fundamental issues that interested MacArthur and Wilson. These include the formation of ecological networks, species abundance distributions, and the contribution of evolution to community assembly. We also extend our prospects to other fields of ecology and evolution - understanding ecosystem functioning, speciation and diversification - frequently employing assets of oceanic islands in inferring the geographic area within which evolution has occurred, and potential barriers to gene flow. Although island-based theory is continually being enriched, incorporating non-equilibrium dynamics is identified as a major challenge for the future.

Timing and number of colonizations but not diversification rates affect diversity patterns in hemosporidian lineages on a remote oceanic archipelago.

Parasite diversity on remote oceanic archipelagos is determined by the number and timing of colonizations and by in situ diversification rate. In this study, we compare intra-archipelago diversity of two hemosporidian parasite genera, Plasmodium and Leucocytozoon, infecting birds of the Mascarene archipelago. Despite the generally higher vagility of Plasmodium parasites, we report a diversity of Plasmodium cytochrome b haplotypes in the archipelago much lower than that of Leucocytozoon. Using phylogenetic data, we find that this difference in diversity is consistent with differences in the timing and number of colonizations, while rates of diversification do not vary significantly between the two genera. The prominence of immigration history in explaining current diversity patterns highlights the importance of historical contingencies in driving disparate biogeographic patterns in potentially harmful blood parasites infecting island birds.

The role of immigration and in-situ radiation in explaining blood parasite assemblages in an island bird clade.

Parasite communities on islands are assembled through multiple immigrations and/or in-situ diversification. In this study, we used a phylogenetic approach to investigate the role of such processes in shaping current patterns of diversity in Leucocytozoon, a group of haemosporidian blood parasites infecting whites eyes (Zosterops) endemic to the Mascarene archipelago (south-western Indian Ocean). We found that this parasite community arose through a combination of multiple immigrations and in-situ diversification, highlighting the importance of both processes in explaining island diversity. Specifically, two highly diverse parasite clades appear to have been present in the Mascarenes for most of their evolutionary history and have diversified within the archipelago, while another lineage apparently immigrated more recently, probably with human-introduced birds. Interestingly, the evolutionary histories of one clade of parasites and Indian Ocean Zosterops seem tightly associated with a significant signal for phylogenetic congruence, suggesting that host-parasite co-divergence may have occurred in this system.

Evidence of multiple colonizations as a driver of black fly diversification in an oceanic island.

True oceanic islands typically host reduced species diversity together with high levels of endemism, which make these environmental set-ups ideal for the exploration of species diversification drivers. In the present study, we used black fly species (Diptera: Simuliidae) from Reunion Island as a model to highlight the main drivers of insect species diversification in this young and remote volcanic island located in the Southwestern Indian Ocean. Using local and regional (Comoros and Seychelles archipelagos) samples as well as specimens from continental Africa, we tested the likelihood of two distinct scenarios, i.e. multiple colonizations vs. in-situ diversification. For this, posterior odds were used to test whether species from Reunion did form a monophyletic group and we estimated divergence times between species. Three out of the four previously described Reunion black fly species could be sampled, namely Simulium ruficorne, Simulium borbonense and Simulium triplex. The phylogenies based on nuclear and mitochondrial markers showed that S. ruficorne and S. borbonense are the most closely related species. Interestingly, we report a probable mitochondrial introgression between these two species although they diverged almost six million years ago. Finally, we showed that the three Reunion species did not form a monophyletic group, and, combined with the molecular datation, the results indicated that Reunion black fly diversity resulted from multiple colonization events. Thus, multiple colonizations, rather than in-situ diversification, are likely responsible for an important part of black fly diversity found on this young Darwinian island.

A novel locus on chromosome 1 underlies the evolution of a melanic plumage polymorphism in a wild songbird.

Understanding the mechanisms responsible for phenotypic diversification within and among species ultimately rests with linking naturally occurring mutations to functionally and ecologically significant traits. Colour polymorphisms are of great interest in this context because discrete colour patterns within a population are often controlled by just a few genes in a common environment. We investigated how and why phenotypic diversity arose and persists in the Zosterops borbonicus white-eye of Reunion (Mascarene archipelago), a colour polymorphic songbird in which all highland populations contain individuals belonging to either a brown or a grey plumage morph. Using extensive phenotypic and genomic data, we demonstrate that this melanin-based colour polymorphism is controlled by a single locus on chromosome 1 with two large-effect alleles, which was not previously described as affecting hair or feather colour. Differences between colour morphs appear to rely upon complex cis-regulatory variation that either prevents the synthesis of pheomelanin in grey feathers, or increases its production in brown ones. We used coalescent analyses to show that, from a 'brown' ancestral population, the dominant 'grey' allele spread quickly once it arose from a new mutation. Since colour morphs are always found in mixture, this implies that the selected allele does not go to fixation, but instead reaches an intermediate frequency, as would be expected under balancing selection.

Mass production of SNP markers in a nonmodel passerine bird through RAD sequencing and contig mapping to the zebra finch genome.

Here, we present an adaptation of restriction-site-associated DNA sequencing (RAD-seq) to the Illumina HiSeq2000 technology that we used to produce SNP markers in very large quantities at low cost per unit in the Réunion grey white-eye (Zosterops borbonicus), a nonmodel passerine bird species with no reference genome. We sequenced a set of six pools of 18-25 individuals using a single sequencing lane. This allowed us to build around 600 000 contigs, among which at least 386 000 could be mapped to the zebra finch (Taeniopygia guttata) genome. This yielded more than 80 000 SNPs that could be mapped unambiguously and are evenly distributed across the genome. Thus, our approach provides a good illustration of the high potential of paired-end RAD sequencing of pooled DNA samples combined with comparative assembly to the zebra finch genome to build large contigs and characterize vast numbers of informative SNPs in nonmodel passerine bird species in a very efficient and cost-effective way.