THE SEX-RATIO TRAIT IN DROSOPHILA SIMULANS: GEOGRAPHICAL DISTRIBUTION OF DISTORTION AND RESISTANCE

The sex-ratio trait we describe here in Drosophila simulans results from X-linked meiotic drive. Males bearing a driving X chromosome can produce a large excess of females (about 90%) in their progeny. This is, however, rarely the case in the wild, where resistance factors, including autosomal suppressors and insensitive Y chromosomes, prevent the expression of the driver. In this study, we searched for drive and resistance factors in strains of Drosophila simulans collected all over the world. Driving X chromosomes were found in all populations whenever a good sample size was available. Their frequency may reach up to 60%. However, the presence of driving X chromosomes never results in an excess of females, due to the systematic co-occurrence of resistance factors. The highest frequencies of driving X chromosomes were observed in islands, while populations from East and Central Africa (the supposed center of origin of the species) showed the highest level of resistance. The geographical pattern of drive and resistance factors, as well as the results of crosses between strains from different geographical areas, suggest that the sex-ratio system described here has a unique and ancient origin in the species.     

Arms race co‐evolution of Magnaporthe oryzae AVR‐Pik and rice Pik genes driven by their physical interactions

Attack and counter‐attack impose strong reciprocal selection on pathogens and hosts, leading to development of arms race evolutionary dynamics. Here we show that Magnaporthe oryzae avirulence gene AVR‐Pik and the cognate rice resistance (R) gene Pik are highly variable, with multiple alleles in which DNA replacements cause amino acid changes. There is tight recognition specificity of the AVR‐Pik alleles by the various Pik alleles. We found that AVR‐Pik physically binds the N‐terminal coiled‐coil domain of Pik in a yeast two‐hybrid assay as well as in an in planta co‐immunoprecipitation assay. This binding specificity correlates with the recognition specificity between AVR and R genes. We propose that AVR‐Pik and Pik are locked into arms race co‐evolution driven by their direct physical interactions.     

Autosomal suppression and fitness costs of an old driving X chromosome in Drosophila testacea

Driving X chromosomes (X^Ds) bias their own transmission through males by killing Y‐bearing gametes. These chromosomes can in theory spread rapidly in populations and cause extinction, but many are found as balanced polymorphisms or as “cryptic” X^Ds shut down by drive suppressors. The relative likelihood of these outcomes and the evolutionary pathways through which they come about are not well understood. An X^D was recently discovered in the mycophagous fly, Drosophila testacea, presenting the opportunity to compare this X^D with the well‐studied X^D of its sister species, Drosophila neotestacea. Comparing features of independently evolved X^Ds in young sister species is a promising avenue towards understanding how X^Ds and their counteracting forces change over time. In contrast to the X^D of D. neotestacea, we find that the X^D of D. testacea is old, with its origin predating the radiation of three species: D. testacea, D. neotestacea and their shared sister species, Drosophila orientacea. Motivated by the suggestion that older X^Ds should be more deleterious to carriers, we assessed the effect of the X^D on both male and female fertility. Unlike what is known from D. neotestacea, we found a strong fitness cost in females homozygous for the X^D in D. testacea: a large proportion of homozygous females failed to produce offspring after being housed with males for several days. Our male fertility experiments show that although X^D male fertility is lower under sperm‐depleting conditions, X^D males have comparable fertility to males carrying a standard X chromosome under a free‐mating regime, which may better approximate conditions in wild populations of D. testacea. Lastly, we demonstrate the presence of autosomal suppression of X chromosome drive. Our results provide support for a model of X^D evolution where the dynamics of young X^Ds are governed by fitness consequences in males, whereas in older X^D systems, both suppression and fitness consequences in females likely supersede male fitness costs.     

Contrasting patterns of X‐chromosome divergence underlie multiple sex‐ratio polymorphisms in stalk‐eyed flies

Sex‐linked segregation distorters cause offspring sex ratios to differ from equality. Theory predicts that such selfish alleles may either go to fixation and cause extinction, reach a stable polymorphism or initiate an evolutionary arms race with genetic modifiers. The extent to which a sex ratio distorter follows any of these trajectories in nature is poorly known. Here, we used X‐linked sequence and simple tandem repeat data for three sympatric species of stalk‐eyed flies (Teleopsis whitei and two cryptic species of T. dalmanni) to infer the evolution of distorting X chromosomes. By screening large numbers of field and recently laboratory‐bred flies, we found no evidence of males with strongly female‐biased sex ratio phenotypes (SR) in one species but high frequencies of SR males in the other two species. In the two species with SR males, we find contrasting patterns of X‐chromosome evolution. T. dalmanni‐1 shows chromosome‐wide differences between sex‐ratio (X^SR) and standard (X^ST) X chromosomes consistent with a relatively old sex‐ratio haplotype based on evidence including genetic divergence, an inversion polymorphism and reduced recombination among X^SR chromosomes relative to X^ST chromosomes. In contrast, we found no evidence of genetic divergence on the X between males with female‐biased and nonbiased sex ratios in T. whitei. Taken with previous studies that found evidence of genetic suppression of sex ratio distortion in this clade, our results illustrate that sex ratio modification in these flies is undergoing recurrent evolution with diverse genomic consequences.     

Lineage‐specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group

Bacterial plasmids can vary from small selfish genetic elements to large autonomous replicons that constitute a significant proportion of total cellular DNA. By conferring novel function to the cell, plasmids may facilitate evolution but their mobility may be opposed by co‐evolutionary relationships with chromosomes or encouraged via the infectious sharing of genes encoding public goods. Here, we explore these hypotheses through large‐scale examination of the association between plasmids and chromosomal DNA in the phenotypically diverse Bacillus cereus group. This complex group is rich in plasmids, many of which encode essential virulence factors (Cry toxins) that are known public goods. We characterized population genomic structure, gene content and plasmid distribution to investigate the role of mobile elements in diversification. We analysed coding sequence within the core and accessory genome of 190 B. cereus group isolates, including 23 novel sequences and genes from 410 reference plasmid genomes. While cry genes were widely distributed, those with invertebrate toxicity were predominantly associated with one sequence cluster (clade 2) and phenotypically defined Bacillus thuringiensis. Cry toxin plasmids in clade 2 showed evidence of recent horizontal transfer and variable gene content, a pattern of plasmid segregation consistent with transfer during infectious cooperation. Nevertheless, comparison between clades suggests that co‐evolutionary interactions may drive association between plasmids and chromosomes and limit wider transfer of key virulence traits. Proliferation of successful plasmid and chromosome combinations is a feature of specialized pathogens with characteristic niches (Bacillus anthracis, B. thuringiensis) and has occurred multiple times in the B. cereus group.     

Transposable elements in individual genotypes of Drosophila simulans

Transposable elements are abundant, dynamic components of the genome that affect organismal phenotypes and fitness. In Drosophila melanogaster, they have increased in abundance as the species spread out of Africa, and different populations differ in their transposable element content. However, very little is currently known about how transposable elements differ between individual genotypes, and how that relates to the population dynamics of transposable elements overall. The sister species of D. melanogaster, D. simulans, has also recently become cosmopolitan, and panels of inbred genotypes exist from cosmopolitan and African flies. Therefore, we can determine whether the differences in colonizing populations are repeated in D. simulans, what the dynamics of transposable elements are in individual genotypes, and how that compares to wild flies. After estimating copy number in cosmopolitan and African D. simulans, I find that transposable element load is higher in flies from cosmopolitan populations. In addition, transposable element load varies considerably between populations, between genotypes, but not overall between wild and inbred lines. Certain genotypes either contain active transposable elements or are more permissive of transposition and accumulate copies of particular transposable elements. Overall, it is important to quantify genotype‐specific transposable element dynamics as well as population averages to understand the dynamics of transposable element accumulation over time.     

Chromosome arm‐specific patterns of polymorphism associated with chromosomal inversions in the major African malaria vector,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 centred on regions of the genome corresponding to three inversions, which are characterized by high values of F_ST, 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.     

At least two indigenous species of the Bemisia tabaci complex are present in Brazil

Bemisia tabaci is one of the most important global agricultural insect pests, being a vector of emerging plant viruses such as begomoviruses and criniviruses that cause serious problems in many countries. Although knowledge of the genetic diversity of B. tabaci populations is important for controlling this pest and understanding viral epidemics, limited information is available on this pest in Brazil. A survey was conducted in different locations of São Paulo and Mato Grosso states, and the phylogenetic relationships of B. tabaci individuals from 43 populations sampled from different hosts were analysed based on partial mitochondrial cytochrome oxidase 1 gene (mtCOI) sequences. According to the recently proposed classification of the B. tabaci complex, which employs the 3.5% mtCOI sequence divergence threshold for species demarcation, most of the specimens collected were found to belong to the Middle East‐Asia Minor 1 species, which includes the invasive populations of the commonly known B biotype, within the Africa/Middle East/Asia Minor high‐level group. Three specimens collected from Solanun gilo and Ipomoea sp. were grouped together and could be classified in the New World species that includes the commonly known A biotype. However, six specimens collected from Euphorbia heterophylla, Xanthium cavanillesii and Glycine maxima could not be classified into any of the 28 previously proposed species, although according to the 11% mtCOI sequence divergence threshold, they belong to the New World high‐level group. These specimens were classified into a new recently proposed species named New World 2 that includes populations from Argentina. Middle East‐Asia Minor 1, New World and New World 2 were differentiated by RFLP analysis of the mtCOI gene using TaqI enzyme. Taq I analysis in silico also differentiates these from Mediterranean species, thus making this method a convenient tool to determine population dynamics, especially critical for monitoring the presence of this exotic pest in Brazil.     

Intra‐specific body size variation in Polistes paper wasps as a response to social parasite pressure

1. Like avian brood parasites, obligate insect social parasites exploit the parental care of a host species to rear their brood, causing an evident loss of host reproductive success. This fitness cost imposes selective pressure on the host to reduce the parasite effect. A possible outcome of an evolutionary arms race is the selection of host morphological counter‐adaptations to resist parasite attacks. 2. We studied host–parasite pairs of Polistes wasps in which the fighting equipment of the parasite's body allows it to enter the host colony. 3. We searched for host morphological traits related to fighting ability that could be considered counter‐adaptations. As a host–parasite co‐evolutionary arms race can only occur where the two lineages co‐exist, we compared morphological traits of hosts belonging to populations with or without parasite pressure. We report that host foundresses belonging to populations under strong parasite pressure have a larger body size than those belonging to populations without parasite pressure. 4. Behavioural experiments carried out to test if an increase in host body size is useful to oppose parasite usurpation show that large body size foundresses exhibit a greater ability of nest defence.     

Effects of predation on real‐time host–parasite coevolutionary dynamics

The impact of community complexity on pairwise coevolutionary dynamics is theoretically dependent on the extent to which species evolve generalised or specialised adaptations to the multiple species they interact with. Here, we show that the bacteria Pseudomonas fluorescens diversifies into defence specialists, when coevolved simultaneously with a virus and a predatory protist, as a result of fitness trade‐offs between defences against the two enemies. Strong bacteria–virus pairwise coevolution persisted, despite strong protist‐imposed selection. However, the arms race dynamic (escalation of host resistance and parasite infectivity ranges) associated with bacteria–virus coevolution broke down to a greater extent in the presence of the protist, presumably through the elevated genetic and demographic costs of increased bacteria resistance ranges. These findings suggest that strong pairwise coevolution can persist even in complex communities, when conflicting selection leads to evolutionary diversification of different defence strategies.     

No evidence for an intragenomic arms race under paternal genome elimination in Planococcus mealybugs

Genomic conflicts arising during reproduction might play an important role in shaping the striking diversity of reproductive strategies across life. Among these is paternal genome elimination (PGE), a form of haplodiploidy which has independently evolved several times in arthropods. PGE males are diploid but transmit maternally inherited chromosomes only, whereas paternal homologues are excluded from sperm. Mothers thereby effectively monopolize the parentage of sons, at the cost of the father's reproductive success. This creates striking conflict between the sexes that could result in a co‐evolutionary arms race between paternal and maternal genomes over gene transmission, yet empirical evidence that such an arms race indeed takes place under PGE is scarce. This study addresses this by testing whether PGE is complete when paternal genotypes are exposed to divergent maternal backgrounds in intraspecific and hybrid crosses of the citrus mealybug, Planococcus citri, and the closely related Planococcus ficus. We determined whether males can transmit genetic information through their sons by tracking inheritance of two traits in a three‐generation pedigree: microsatellite markers and sex‐specific pheromone preferences. Our results suggest leakages of single paternal chromosomes through males occurring at a low frequency, but we find no evidence for transmission of paternal pheromone preferences from fathers to sons. The absence of differences between hybrid and intraspecific crosses in leakage rate of paternal alleles suggests that a co‐evolutionary arms race cannot be demonstrated on this evolutionary timescale, but we conclude that there is scope for intragenomic conflict between parental genomes in mealybugs. Finally, we discuss how these paternal escapes can occur and what these findings may reveal about the evolutionary dynamics of this bizarre genetic system.     

Oceanographic barriers,divergence, and admixture: Phylogeography and taxonomy of two putative subspecies of short‐finned pilot whale

Genomic phylogeography plays an important role in describing evolutionary processes and their geographic, ecological, or cultural drivers. These drivers are often poorly understood in marine environments, which have fewer obvious barriers to mixing than terrestrial environments. Taxonomic uncertainty of some taxa (e.g., cetaceans), due to the difficulty in obtaining morphological data, can hamper our understanding of these processes. One such taxon, the short‐finned pilot whale, is recognized as a single global species but includes at least two distinct morphological forms described from stranding and drive hunting in Japan, the “Naisa” and “Shiho” forms. Using samples (n = 735) collected throughout their global range, we examine phylogeographic patterns of divergence by comparing mitogenomes and nuclear SNP loci. Our results suggest three types within the species: an Atlantic Ocean type, a western/central Pacific and Indian Ocean (Naisa) type, and an eastern Pacific Ocean and northern Japan (Shiho) type. mtDNA control region differentiation indicates these three types form two subspecies, separated by the East Pacific Barrier: Shiho short‐finned pilot whale, in the eastern Pacific Ocean and northern Japan, and Naisa short‐finned pilot whale, throughout the remainder of the species' distribution. Our data further indicate two diverging populations within the Naisa subspecies, in the Atlantic Ocean and western/central Pacific and Indian Oceans, separated by the Benguela Barrier off South Africa. This study reveals a process of divergence and speciation within a globally‐distributed, mobile marine predator, and indicates the importance of the East Pacific Barrier to this evolutionary process.     

Experimental evidence of genome‐wide impact of ecological selection during early stages of speciation‐with‐gene‐flow

Theory predicts that speciation‐with‐gene‐flow is more likely when the consequences of selection for population divergence transitions from mainly direct effects of selection acting on individual genes to a collective property of all selected genes in the genome. Thus, understanding the direct impacts of ecologically based selection, as well as the indirect effects due to correlations among loci, is critical to understanding speciation. Here, we measure the genome‐wide impacts of host‐associated selection between hawthorn and apple host races of Rhagoletis pomonella (Diptera: Tephritidae), a model for contemporary speciation‐with‐gene‐flow. Allele frequency shifts of 32 455 SNPs induced in a selection experiment based on host phenology were genome wide and highly concordant with genetic divergence between co‐occurring apple and hawthorn flies in nature. This striking genome‐wide similarity between experimental and natural populations of R. pomonella underscores the importance of ecological selection at early stages of divergence and calls for further integration of studies of eco‐evolutionary dynamics and genome divergence.     

Male‐killer dynamics in Danaus chrysippus (L.) (Lepidoptera: Nymphalidae) in East Africa

Within certain regions in East Africa, the butterfly Danaus chrysippus (L.) shows female‐biased population sex ratio, because of the production by some females of all‐female broods, as a result of infection by maternally inherited, male‐killing bacterium of the genus Spiroplasma. In this study, we describe a 3‐year field survey for the population dynamics of the male‐killing Spiroplasma in D. chrysippus in four independent localities, namely Uganda, Ghana, Sudan and Madagascar. The prevalence of the bacterium was found to show extensive variations at multiple scales among different sites, in various countries, seasons and years. A novel, selection‐based hypothesis was suggested to explain the high variability of male‐killer prevalence over space and time, based on the existence of an adaptive link between larval food‐plant density and the magnitude of resource reallocation fitness advantage for the male‐killer.     

Global genetic diversity of Aedes aegypti

Mosquitoes, especially Aedes aegypti, are becoming important models for studying invasion biology. We characterized genetic variation at 12 microsatellite loci in 79 populations of Ae. aegypti from 30 countries in six continents, and used them to infer historical and modern patterns of invasion. Our results support the two subspecies Ae. aegypti formosus and Ae. aegypti aegypti as genetically distinct units. Ae. aegypti aegypti populations outside Africa are derived from ancestral African populations and are monophyletic. The two subspecies co‐occur in both East Africa (Kenya) and West Africa (Senegal). In rural/forest settings (Rabai District of Kenya), the two subspecies remain genetically distinct, whereas in urban settings, they introgress freely. Populations outside Africa are highly genetically structured likely due to a combination of recent founder effects, discrete discontinuous habitats and low migration rates. Ancestral populations in sub‐Saharan Africa are less genetically structured, as are the populations in Asia. Introduction of Ae. aegypti to the New World coinciding with trans‐Atlantic shipping in the 16th to 18th centuries was followed by its introduction to Asia in the late 19th century from the New World or from now extinct populations in the Mediterranean Basin. Aedes mascarensis is a genetically distinct sister species to Ae. aegypti s.l. This study provides a reference database of genetic diversity that can be used to determine the likely origin of new introductions that occur regularly for this invasive species. The genetic uniqueness of many populations and regions has important implications for attempts to control Ae. aegypti, especially for the methods using genetic modification of populations.     

Hot spots become cold spots: coevolution in variable temperature environments

Antagonistic coevolution between hosts and parasites is a key process in the genesis and maintenance of biological diversity. Whereas coevolutionary dynamics show distinct patterns under favourable environmental conditions, the effects of more realistic, variable conditions are largely unknown. We investigated the impact of a fluctuating environment on antagonistic coevolution in experimental microcosms of Pseudomonas fluorescens SBW25 and lytic phage SBWΦ2. High‐frequency temperature fluctuations caused no deviations from typical coevolutionary arms race dynamics. However, coevolution was stalled during periods of high temperature under intermediate‐ and low‐frequency fluctuations, generating temporary coevolutionary cold spots. Temperature variation affected population density, providing evidence that eco‐evolutionary feedbacks act through variable bacteria–phage encounter rates. Our study shows that environmental fluctuations can drive antagonistic species interactions into and out of coevolutionary cold and hot spots. Whether coevolution persists or stalls depends on the frequency of change and the environmental optima of both interacting players.     

The potential for arms race and Red Queen coevolution in a protist host–parasite system

The dynamics and consequences of host–parasite coevolution depend on the nature of host genotype‐by‐parasite genotype interactions (G × G) for host and parasite fitness. G × G with crossing reaction norms can yield cyclic dynamics of allele frequencies (“Red Queen” dynamics) while G × G where the variance among host genotypes differs between parasite genotypes results in selective sweeps (“arms race” dynamics). Here, we investigate the relative potential for arms race and Red Queen coevolution in a protist host–parasite system, the dinoflagellate Alexandrium minutum and its parasite Parvilucifera sinerae. We challenged nine different clones of A. minutum with 10 clones of P. sinerae in a fully factorial design and measured infection success and host and parasite fitness. Each host genotype was successfully infected by four to ten of the parasite genotypes. There were strong G × Gs for infection success, as well as both host and parasite fitness. About three quarters of the G × G variance components for host and parasite fitness were due to crossing reaction norms. There were no general costs of resistance or infectivity. We conclude that there is high potential for Red Queen dynamics in this host–parasite system.     

Eco‐evolutionary dynamics in a coevolving host–virus system

Eco‐evolutionary dynamics have been shown to be important for understanding population and community stability and their adaptive potential. However, coevolution in the framework of eco‐evolutionary theory has not been addressed directly. Combining experiments with an algal host and its viral parasite, and mathematical model analyses we show eco‐evolutionary dynamics in antagonistic coevolving populations. The interaction between antagonists initially resulted in arms race dynamics (ARD) with selective sweeps, causing oscillating host–virus population dynamics. However, ARD ended and populations stabilised after the evolution of a general resistant host, whereas a trade‐off between host resistance and growth then maintained host diversity over time (trade‐off driven dynamics). Most importantly, our study shows that the interaction between ecology and evolution had important consequences for the predictability of the mode and tempo of adaptive change and for the stability and adaptive potential of populations.     

A multi‐genome analysis approach enables tracking of the invasion of a single Russian wheat aphid (Diuraphis noxia) clone throughout the New World

This study investigated the population genetics, demographic history and pathway of invasion of the Russian wheat aphid (RWA) from its native range in Central Asia, the Middle East and Europe to South Africa and the Americas. We screened microsatellite markers, mitochondrial DNA and endosymbiont genes in 504 RWA clones from nineteen populations worldwide. Following pathway analyses of microsatellite and endosymbiont data, we postulate that Turkey and Syria were the most likely sources of invasion to Kenya and South Africa, respectively. Furthermore, we found that one clone transferred between South Africa and the Americas was most likely responsible for the New World invasion. Finally, endosymbiont DNA was found to be a high‐resolution population genetic marker, extremely useful for studies of invasion over a relatively short evolutionary history time frame. This study has provided valuable insights into the factors that may have facilitated the recent global invasion by this damaging pest.     

Paternal lineages in Libya inferred from Y‐chromosome haplogroups

Many studies based on genetic diversity of North African populations have contributed to elucidate the modelling of the genetic landscape in this region. North Africa is considered as a distinct spatial‐temporal entity on geographic, archaeological, and historical grounds, which has undergone the influence of different human migrations along its shaping. For instance, Libya, a North African country, was first inhabited by Berbers and then colonized by a variety of ethnic groups like Phoenicians, Greeks, Romans, Arabs and, in recent times, Italians. In this study, we contribute to clarify the genetic variation of Libya and consequently, of North African modern populations, by the study of Libyan male lineages. A total of 22 Y‐chromosome‐specific SNPs were genotyped in a sample of 175 Libyan males, allowing the characterization of 18 Y‐chromosomal haplogroups. The obtained data revealed a predominant Northwest African component represented by haplogroup E‐M81 (33.7%) followed by J(xJ1a,J2)‐M304 (27.4%), which is postulated to have a Middle Eastern origin. The comparative study with other populations (～5,400 individuals from North Africa, Middle East, Sub‐Saharan Africa, and Europe) revealed a general genetic homogeneity among North African populations (F_ST = 5.3 %; P‐value < 0.0001). Overall, the Y‐haplogroup diversity in Libya and in North Africa is characterized by two genetic components. The first signature is typical of Berber‐speaking people (E‐M81), the autochthonous inhabitants, whereas the second is (J(xJ1a,J2)‐M304), originating from Arabic populations. This is in agreement with the hypothesis of an Arabic expansion from the Middle East, shaping the North African genetic landscape. Am J Phys Anthropol 157:242–251, 2015. © 2015 Wiley Periodicals, Inc.