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bioRxiv2016

Pollutants and insecticides drive local adaptation in African malaria mosquitoes

The Anopheles gambiae complex contains a number of highly anthropophilic mosquito species that have acquired exceptional ability to thrive in complex human habitats. Thus, examining the evolutionary history of this Afrotropical mosquito may yield vital information on the selective processes that occurred during the adaptation to human-dominated environments. We performed reduced representation sequencing on 941 mosquitoes of the Anopheles gambiae complex collected across four ecogeographic zones in Cameroon. We find evidence for genetic and geographic subdivision within An. coluzzii and An. gambiae sensu stricto - the two most significant malaria vectors in the region. Importantly, in both species, rural and urban populations are genetically differentiated. Genome scans reveal pervasive signatures of selection centered on genes involved in xenobiotic resistance. Notably, a selective sweep containing detoxification enzymes is prominent in urban mosquitoes that exploit polluted breeding sites. Overall, our study suggests that recent anthropogenic environmental modifications and widespread use of insecticides are driving population differentiation and local adaptation in vectors with potentially significant consequences for malaria epidemiology.

Evolutionary Biology↗

bioRxiv2016

Genetic Diversity, Population Structure and Species Delimitation of Trialeurodes vaporariorum (Greenhouse whitefly)

Genetic diversity within Trialeurodes vaporariorum (Westwood, 1856) remains largely unexplored, particularly within regions of Sub-Saharan Africa. In this study, T. vaporariorum samples were obtained from three locations in Kenya: Katumani, Kiambu and Kajiado counties. DNA extraction, PCR and Sanger sequencing were carried out on ~750 bp fragment of the mitochondria cytochrome c oxidase I (COI) gene from individual whiteflies. In addition, global populations were assessed and 19 haplotypes were identified, with three main haplotypes (Hp_19, Hp_10, Hp_011) circulating within Kenya. Measures of genetic diversity among T. vaporariorum populations resulted in haplotype diversity of 0.411, nucleotide diversity 0.00096, and Tajimas D -0. 30315, (P>0.10). Analysis of population structure across global sequences using Structurama indicated one population globally, with posterior probability of 0.72. Bayesian and maximum likelihood phylogenetic analysis gave support for two clades (Clade I = an admixed global population and Clade II = subset of Kenyan and 1 Greek sequence). Species delimitation between the two clades was assessed by four parameters; posterior probability, Kimuras two parameter (K2P), Rodrigos P (Randomly distinct) and Rosenbergs reciprocal monophyly (P(AB). The two clades within the phylogenetic tree showed evidence of distinctness based on; Kimura two parameters (K2P) (p = -1.21E-01), Rodrigos P (RD) (p =0.05) and Rosenbergs P(AB) (p = 2.3E -13). Overall, low genetic diversity within the Kenyan samples is a likely indicator of recent population expansion and colonization with this region and plausible signs of species complex formation in Sub-Saharan Africa.

Evolutionary Biology↗

bioRxiv2016

Recombination-driven genome evolution and stability of bacterial species

While bacteria divide clonally, horizontal gene transfer followed by homologous recombination is now recognized as an important and sometimes even dominant contributor to their evolution. However, the details of how the competition between clonal inheritance and recombination shapes genome diversity, population structure, and species stability remains poorly understood. Using a computational model, we find two principal regimes in bacterial evolution and identify two composite parameters that dictate the evolutionary fate of bacterial species. In the divergent regime, characterized by either a low recombination frequency or strict barriers to recombination, cohesion due to recombination is not sufficient to overcome the mutational drift. As a consequence, the divergence between any pair of genomes in the population steadily increases in the course of their evolution. The species as a whole lacks genetic coherence with sexually isolated clonal sub-populations continuously formed and dissolved. In contrast, in the metastable regime, characterized by a high recombination frequency combined with low barriers to recombination, genomes continuously recombine with the rest of the population. The population remains genetically cohesive and stable over time. The transition between these two regimes can be affected by relatively small changes in evolutionary parameters. Using the Multi Locus Sequence Typing (MLST) data we classify a number of well-studied bacterial species to be either the divergent or the metastable type. Generalizations of our framework to include fitness and selection, ecologically structured populations, and horizontal gene transfer of non-homologous regions are discussed.

Evolutionary Biology↗

bioRxiv2016

Evolution of simple multicellularity increases environmental complexity

Multicellularity--the integration of previously autonomous cells into a new, more complex organism--is one of the major transitions in evolution. Multicellularity changed evolutionary possibilities and facilitated the evolution of increased complexity. Transitions to multicellularity are associated with rapid diversification and increased ecological opportunity but the potential mechanisms are not well understood. In this paper we explore the ecological mechanisms of multicellular diversification during experimental evolution of the brewers yeast, Saccharomyces cerevisiae. The evolution from single cells into multicellular clusters modifies the structure of the environment, changing the fluid dynamics and creating novel ecological opportunities. This study demonstrates that even in simple conditions, incipient multicellularity readily changes the environment, facilitating the origin and maintenance of diversity.

Evolutionary Biology↗

bioRxiv2016

Testing for local adaptation and evolutionary potential along altitudinal gradients in rainforest Drosophila: limitations of laboratory estimates.

Predicting how species will respond to the rapid climatic changes predicted this century is an urgent task. Species Distribution Models (SDMs) use the current relationship between environmental variation and species abundances to predict the effect of future environmental change on their distributions. However, two common assumptions of SDMs are likely to be violated in many cases: (1) that the relationship of environment with abundance or fitness is constant throughout a species range and will remain so in future, and (2) that abiotic factors (e.g. temperature, humidity) determine species distributions. We test these assumptions by relating field abundance of the rainforest fruit fly Drosophila birchii to ecological change across gradients that include its low and high altitudinal limits. We then test how such ecological variation affects the fitness of 35 D. birchii families transplanted in 591 cages to sites along two altitudinal gradients, to determine whether genetic variation in fitness responses could facilitate future adaptation to environmental change. Overall, field abundance was highest at cooler, high altitude sites, and declined towards warmer, low altitude sites. By contrast, cage fitness (productivity) increased towards warmer, lower altitude sites, suggesting that biotic interactions (absent from cages) drive ecological limits at warmer margins. In addition, the relationship between environmental variation and abundance varied significantly among gradients, indicating divergence in ecological niche across the species range. However, there was no evidence for local adaptation within gradients, despite greater productivity of high altitude than low altitude populations when families were reared under laboratory conditions. Families also responded similarly to transplantation along gradients, providing no evidence for fitness trade-offs that would favour local adaptation. These findings highlight the importance of (1) measuring genetic variation of key traits under ecologically relevant conditions, and (2) considering the effect of biotic interactions when predicting species responses to environmental change.

Evolutionary Biology↗

bioRxiv2016

Chromosomal inversions facilitate chromosome-scale evolution in Anopheles funestus

Chromosomal inversions facilitate local adaptation of beneficial mutations and modulate genetic polymorphism, but the extent of their effects within the genome is still insufficiently understood. The genome of Anopheles funestus, a malaria mosquito endemic to sub-Saharan Africa, contains an impressive number of paracentric polymorphic inversions, which are unevenly distributed among chromosomes and provide an excellent framework for investigating the genomic impacts of chromosomal rearrangements. Here we present results of a fine-scale analysis of genetic variation within the genome of two weakly differentiated populations of Anopheles funestus inhabiting contrasting moisture conditions in Cameroon. Using population genomic analyses, we found that genetic divergence between the two populations is centered on regions of the genome corresponding to three inversions, which are characterized by high values of FST, absolute sequence divergence and fixed differences. Importantly, in contrast to the 2L chromosome arm, which is collinear, nucleotide diversity is significantly reduced along the entire length of three autosome arms bearing multiple overlapping chromosomal rearrangements. These findings support the idea that interactions between reduced recombination and natural selection within inversions contribute to sculpt nucleotide polymorphism across chromosomes in An. funestus.

Evolutionary Biology↗

bioRxiv2016

Rapid expansion of immune-related gene families in the house fly, Musca domestica

The house fly, Musca domestica, occupies an unusual diversity of potentially septic niches among sequenced Dipteran insects and is a vector of numerous diseases of humans and livestock. In the present study, we apply whole-transcriptome sequencing to identify genes whose expression is regulated in adult flies by bacterial infection. We then combine the transcriptomic data with analysis of rates of gene duplication and loss to provide insight into the evolutionary dynamics of immune-related genes. Genes up-regulated after bacterial infection are biased toward being evolutionarily recent innovations, suggesting the recruitment of novel immune components in the M. domestica or ancestral Dipteran lineages. In addition, using new models of gene family evolution, we show that several different classes of immune-related genes, particularly those involved in either pathogen recognition or pathogen killing, are duplicating at a significantly accelerated rate on the M. domestica lineage relative to other Dipterans. Taken together, these results suggest that the M. domestica immune response includes an unusual diversity of genes, perhaps as a consequence of its lifestyle in septic environments.

Evolutionary Biology↗

bioRxiv2016

Genomic signatures of introgression at late stages of speciation in a malaria mosquito

Ongoing speciation in most African malaria vectors gives rise to cryptic populations, which differ remarkably in their behaviour, ecology and capacity to vector malaria parasites. Understanding the population structure and the drivers of genetic differentiation among mosquitoes is critical for effective disease control because heterogeneity within species contribute to variability in malaria cases and allow fractions of vector populations to escape control efforts. To examine the population structure and the potential impacts of recent large-scale control interventions, we have investigated the genomic patterns of differentiation in mosquitoes belonging to the Anopheles nili group, a large taxonomic group that diverged [~]3-Myr ago. Using 4343 single nucleotide polymorphisms (SNPs), we detected strong population structure characterized by high FST values between multiple divergent populations adapted to different habitats within the Central African rainforest. Delineating the cryptic species within the Anopheles nili group is challenging due to incongruence between morphology, ribosomal DNA and SNP markers consistent with incomplete lineage sorting and/or interspecific gene flow. A very high proportion of loci are fixed (FST = 1) within the genome of putative species, which suggests that ecological and/or reproductive barriers are maintained by strong selection on a substantial number of genes.

Evolutionary Biology↗

bioRxiv2016

Extensive genetic diversity among populations of the malaria mosquito Anopheles moucheti revealed by population genomics

Malaria vectors are exposed to intense selective pressures due to large-scale intervention programs that are underway in most African countries. One of the current priorities is therefore to clearly assess the adaptive potential of Anopheline populations, which is critical to understand and anticipate the response mosquitoes can elicit against such adaptive challenges. The development of genomic resources that will empower robust examinations of evolutionary changes in all vectors including currently understudied species is an inevitable step toward this goal. Here we constructed double-digest Restriction Associated DNA (ddRAD) libraries and generated 6461 Single Nucleotide Polymorphisms (SNPs) that we used to explore the population structure and demographic history of wild-caught Anopheles moucheti from Cameroon. The genome-wide distribution of allelic frequencies among samples best fitted that of an old population at equilibrium, characterized by a weak genetic structure and extensive genetic diversity, presumably due to a large long term effective population size. Estimates of FST and Linkage Disequilibrium (LD) across SNPs reveal a very low genetic differentiation throughout the genome and the absence of segregating LD blocks among populations, suggesting an overall lack of local adaptation. Our study provides the first investigation of the genetic structure and diversity in An. moucheti at the genomic scale. We conclude that, despite a weak genetic structure, this species has the potential to challenge current vector control measures and other rapid anthropogenic and environmental changes thanks to its great genetic diversity.

Evolutionary Biology↗

bioRxiv2016

Dynamics and fate of beneficial mutations under lineage contamination by linked deleterious mutations

Beneficial mutations drive adaptive evolution, yet their selective advantage does not ensure their fixation. Haldanes application of single-type branching process theory showed that genetic drift alone could cause the extinction of newly-arising beneficial mutations with high probability. With linkage, deleterious mutations will affect the dynamics of beneficial mutations and might further increase their extinction probability. Here, we model the lineage dynamics of a newly-arising beneficial mutation as a multitype branching process; this approach allows us to account for the combined effects of drift and the stochastic accumulation of linked deleterious mutations, which we call lineage contamination. We first study the lineage contamination phenomenon in isolation, deriving extinction times and probabilities of beneficial lineages. We then put the lineage contamination phenomenon into the context of an evolving population by incorporating the effects of background selection. We find that the survival probability of beneficial mutations is simply Haldanes classical formula multiplied by the correction factor [Formula], where U is deleterious mutation rate, [Formula] is mean selective advantage of beneficial mutations,{kappa} [isin] (1,{varepsilon} ], and{varepsilon} = 2 - e-1. We also find there exists a genomic deleterious mutation rate, [Formula], that maximizes the rate of production of surviving beneficial mutations, and that [Formula]. Both of these results, and others, are curiously independent of the fitness effects of deleterious mutations. We derive critical mutation rates above which: 1) lineage contamination alleviates competition among beneficial mutations, and 2) the adaptive substitution process all but shuts down.

Evolutionary Biology↗

bioRxiv2016

Population structure reduces the benefits from partner choice in mutualism

Mutualisms are key drivers of evolutionary and ecological processes. Understanding how different species can evolve to interact in mutually beneficial ways is an important goal of evolutionary theory, especially when the benefits require costly investments by the partners. For such costly investments to evolve, some sort of fitness feedback mechanism must exist that more than recoups the direct costs. Several such feedback mechanisms have been explored both theoretically and empirically, yet we know relatively little how they might act together, as they probably do in nature. In this paper, I model the joint action of three of the main mechanisms that can maintain symbiotic cooperation: partner choice by hosts, population structure amongst symbionts, and undirected rewards from hosts to symbionts. My results show that population structure reduces the benefit from partner choice to hosts. It may help or hinder beneficial symbionts and create positive or negative frequency dependence depending on the nature of host rewards to the symbiont. Strong population structure also makes it less likely that host choosiness and symbiont cooperation will be jointly maintained in a population. The intuition behind my results is that all else being equal, population structure reduces local variation available to the host to choose from. Thus, population structure is not always beneficial for the evolution of cooperation between species. My results also underscore the need to do full analyses of multiple mechanisms of social evolution to uncover their interactions to uncover the interactions between them.

Evolutionary Biology↗

bioRxiv2016

The frequency spectrum of chromatin accessibility in Yorubans points toward a significant role of random genetic drift in shaping the chromatin landscape

The function of non-coding variation in the human genome is hotly debated. While much of the genome appears to be involved in some kind of molecular activity, a relatively small portion of the genome appears to be conserved across mammalian species. To try to understand part of this seeming paradox, we examined chromatin accessibility as a model molecular phenotype. We modeled chromatin state as either open or closed as looked at the frequency of open chromatin across 70 Yoruban cell lines. We saw that most regions of chromatin accessibility occurred in only a small number of individuals, although there are a number of regions that are accessible across the entire panel. To delve further into understanding the evolutionary mechanisms, we examined nucleotide diversity in and around accessible regions. We found that in the open chromatin access, low frequency regions had decreased nucleotide diversity, however, they were situated within regions of elevated nucleotide diversity. These results point toward a role of random mutation and genetic drift shaping the distribution of accessible regions in the human genome.

Evolutionary Biology↗

bioRxiv2016

Modeling the multiple facets of speciation-with-gene-flow towards improving divergence history inference of a recent fish adaptive radiation.

Parallel divergence patterns across replicated species pairs occurring in similar environmental contrasts may arise through distinct evolutionary scenarios. Deciphering whether such parallelism actually reflects repeated parallel divergence driven by divergent selection or a single divergence event with subsequent gene flow needs to be ascertained. Reconstructing historical gene flow is therefore of fundamental interest to understand how demography and selection jointly shaped genomic divergence during speciation. Here, we use an extended modeling framework to explore the multiple facets of speciation-with-gene-flow with demo-genetic divergence models that capture both temporal and genomic variation in effective population size and migration rate. We investigate the divergence history of five sympatric Lake Whitefish limnetic (dwarf) and benthic (normal) species pairs characterized by variable degrees of ecological divergence and reproductive isolation. Genome-wide SNPs were used to document the extent of genetic differentiation in each species pair, and 26 divergence models were fitted and compared to the unfolded joint allele frequency spectrum of each pair. We found evidence that a recent (circa 3000-4000 generations) asymmetrical secondary contact between expanding post-glacial populations has accompanied Whitefish diversification. Our results suggest that heterogeneous genomic differentiation patterns have emerged through the combined effects of linked selection generating variable rates of lineage sorting across the genome during geographical isolation, and heterogeneous introgression eroding divergence at different rates across the genome upon secondary contact. This study thus provides a new retrospective insight into the historical demographic and selective processes that shaped a continuum of divergence associated with ecological speciation.

Evolutionary Biology↗

bioRxiv2016

Phylogenomic Analysis of Ants, Bees and Stinging Wasps: Improved Taxon Sampling Enhances Understanding of Hymenopteran Evolution

The importance of taxon sampling in phylogenetic accuracy is a topic of active debate. We investigated the role of taxon sampling in causing incongruent results between two recent phylogenomic studies of stinging wasps (Hymenoptera: Aculeata), a diverse lineage that includes ants, bees and the majority of eusocial insects. Using target enrichment of ultraconserved element (UCE) loci, we assembled the largest aculeate phylogenomic data set to date, sampling 854 loci from 187 taxa, including 30 out of 31 aculeate families, and a diversity of parasitoid outgroups. We analyzed the complete matrix using multiple analytical approaches, and also performed a series of taxon inclusion/exclusion experiments, in which we analyzed taxon sets identical to and slightly modified from the previous phylogenomic studies. Our results provide a highly supported phylogeny for virtually all aculeate lineages sampled, supporting ants as sister to Apoidea (bees+apoid wasps), bees as sister to Philanthinae+Pemphredoninae (lineages within a paraphyletic Crabronidae), Melittidae as sister to remaining bees, and paraphyly of cuckoo wasps (Chrysidoidea). Our divergence dating analyses estimate ages for aculeate lineages in close concordance with the fossil record. Our analyses also demonstrate that outgroup choice and taxon evenness can fundamentally impact topology and clade support in phylogenomic inference.

Evolutionary Biology↗

bioRxiv2016

Exploring evolutionary relationships across the genome using topology weighting

We introduce the concept of topology weighting, a method for quantifying relationships between taxa that are not necessarily monophyletic, and visualising how these relationships change across the genome. A given set of taxa can be related in a limited number of ways, but if each taxon is represented by multiple sequences, the number of possible topologies becomes very large. Topology weighting reduces this complexity by quantifying the contribution of each 'taxon topology' to the full tree. We describe our method for topology weighting by iterative sampling of sub-trees (Twisst), and test it on both simulated and real genomic data. Overall, we show that this is an informative and versatile approach, suitable for exploring relationships in almost any genomic dataset.\n\nScripts to implement the method described are available at github.com/simonhmartin/twisst.

Evolutionary Biology↗

bioRxiv2016

Gene-culture co-inheritance of a behavioral trait.

Human behavioral traits are complex phenotypes that result from both genetic and cultural transmission. But different inheritance systems need not favor the same phenotypic outcome. What happens when there are conflicting selection forces in the two domains? To address this question, we derive a Price equation that incorporates both cultural and genetic inheritance of a phenotype where the effects of genes and culture are additive. We then use this equation to investigate whether a genetically maladaptive phenotype can evolve under dual transmission. We examine the special case of altruism using an illustrative model, and show that cultural selection can overcome genetic selection when the variance in culture is sufficiently high with respect to genes. Finally, we show how our basic result can be extended to non-additive effects models. We discuss the implications of our results for understanding the evolution of maladaptive behaviors.

Evolutionary Biology↗

bioRxiv2016

A functional analysis of the contribution of climatic niche divergence to adaptive radiation

Elucidating how ecological and evolutionary mechanisms interact to produce and maintain biodiversity is a fundamental problem in evolutionary ecology. We investigate this issue by focusing on how physiological evolution affects performance and species coexistence along the thermal niche axis in replicated radiations of Anolis lizards, groups best known for resource partitioning based on morphological divergence. We find repeated divergence in thermal physiology within these radiations, and that this divergence significantly affects performance within natural thermal environments. Morphologically similar species that co-occur invariably differ in their thermal physiology, providing evidence that physiological divergence facilitates species co-existence within anole communities. Despite repeated divergence in traits of demonstrable ecological importance, phylogenetic comparative analyses indicate that physiological traits have evolved more slowly than key morphological traits related to the structural niche. Phylogenetic analyses also reveal that physiological divergence is correlated with divergence in broad-scale habitat climatic features commonly used to estimate thermal niche evolution, but that the latter incompletely predicts variation in the former. We provide comprehensive evidence for repeated adaptive evolution of physiological divergence within Anolis adaptive radiations, including the complementary roles of physiological and morphological divergence in promoting community-level diversity. We recommend greater integration of performance-based traits into analyses of climatic niche evolution, as they facilitate a more complete understanding of the phenotypic and ecological consequences of climatic divergence.

Evolutionary Biology↗

bioRxiv2016

Genome-scale rates of evolutionary change in bacteria

Estimating the rates at which bacterial genomes evolve is critical to understanding major evolutionary and ecological processes such as disease emergence, long-term host-pathogen associations, and short-term transmission patterns. The surge in bacterial genomic data sets provides a new opportunity to estimate these rates and reveal the factors that shape bacterial evolutionary dynamics. For many organisms estimates of evolutionary rate display an inverse association with the time-scale over which the data are sampled. However, this relationship remains unexplored in bacteria due to the difficulty in estimating genome-wide evolutionary rates, which are impacted by the extent of temporal structure in the data and the prevalence of recombination. We collected 36 whole genome sequence data sets from 16 species of bacterial pathogens to systematically estimate and compare their evolutionary rates and assess the extent of temporal structure in the absence of recombination. The majority (28/36) of data sets possessed sufficient clock-like structure to robustly estimate evolutionary rates. However, in some species reliable estimates were not possible even with \"ancient DNA\" data sampled over many centuries, suggesting that they evolve very slowly or that they display extensive rate variation among lineages. The robustly estimated evolutionary rates spanned several orders of magnitude, from 10-6 to 10-8 nucleotide substitutions site-1 year-1. This variation was largely attributable to sampling time, which was strongly negatively associated with estimated evolutionary rates, with this relationship best described by an exponential decay curve. To avoid potential estimation biases such time-dependency should be considered when inferring evolutionary time-scales in bacteria.

Evolutionary Biology↗