Rapid Sequential Spread of Two Wolbachia Variants in Drosophila simulans

The maternally inherited intracellular bacteria Wolbachia can manipulate host reproduction in various ways that foster frequency increases within and among host populations. Manipulations involving cytoplasmic incompatibility (CI), where matings between infected males and uninfected females produce non-viable embryos, are common in arthropods and produce a reproductive advantage for infected females. CI was associated with the spread of Wolbachia variant wRi in Californian populations of Drosophila simulans, which was interpreted as a bistable wave, in which local infection frequencies tend to increase only once the infection becomes sufficiently common to offset imperfect maternal transmission and infection costs. However, maternally inherited Wolbachia are expected to evolve towards mutualism, and they are known to increase host fitness by protecting against infectious microbes or increasing fecundity. We describe the sequential spread over approximately 20 years in natural populations of D. simulans on the east coast of Australia of two Wolbachia variants (wAu and wRi), only one of which causes significant CI, with wRi displacing wAu since 2004. Wolbachia and mtDNA frequency data and analyses suggest that these dynamics, as well as the earlier spread in California, are best understood as Fisherian waves of favourable variants, in which local spread tends to occur from arbitrarily low frequencies. We discuss implications for Wolbachia-host dynamics and coevolution and for applications of Wolbachia to disease control.     

EVOLUTION OF INCOMPATIBILITY-INDUCING MICROBES AND THEIR HOSTS

In many insect species, males infected with microbes related to Wolbachia pipientis are “incompatible” with uninfected females. Crosses between infected males and uninfected females produce significantly fewer adult progeny than the other three possible crosses. The incompatibility-inducing microbes are usually maternally transmitted. Thus, incompatibility tends to confer a reproductive advantage on infected females in polymorphic populations, allowing these infections to spread. This paper analyzes selection on parasite and host genes that affect such incompatibility systems. Selection among parasite variants does not act directly on the level of incompatibility with uninfected females. In fact, selection favors rare parasite variants that increase the production of infected progeny by infected mothers, even if these variants reduce incompatibility with uninfected females. However, productivity-reducing parasites that cause partial incompatibility with hosts harboring alternative variants can be favored once they become sufficiently abundant locally. Thus, they may spread spatially by a process analogous to the spread of underdominant chromosome rearrangements. The dynamics of modifier alleles in the host are more difficult to predict, because such alleles will occur in both infected and uninfected individuals. Nevertheless, the relative fecundity of infected females compared to uninfected females, the efficiency of maternal transmission and the mutual compatibility of infected individuals all tend to increase under within-population selection on both host and parasite genes. In addition, selection on host genes favors increased compatibility between infected males and uninfected females. Although vertical transmission tends to harmonize host and parasite evolution, competition among parasite variants will tend to maintain incompatibility.     

Evaluating spread of invaders from gravity scores - A way of using gravity models in ecology

This study is a theoretical excursion into gravity models and their usability in evaluating importance of spatial structure and population development for the spread of colonizing organisms. A so called “gravity score” for sites is deduced, and such a score could be used for predicting risk of colonization once one site in an area has been subject to introduction of a new species. The analysis further suggests that factors deciding spread between sites differs from those that govern expected population sizes. Gravity models of the kind presented here includes both population dynamics and spatial structure and could be a complement to other models describing organism spread.     

Long-term persistence of exaggerated ornaments under Fisherian runaway despite costly mate search

Exaggerated ornaments often evolve due to the mating preferences of the opposite sex. Genetic correlations between preferences and ornaments can lead both traits to elaborate dramatically in tandem, in a process known as ‘Fisherian runaway’. However, in most previous models of Fisherian runaway, elaborate ornaments are not expected to persist when preferences are consistently costly to the choosing sex. In contrast, we show here that exaggerated male ornaments can be maintained long term even when females must pay a cost to choose their mates. Preferences per se are not costly in our model, but females can only act on their preferences by investing resources in mate search. We predict that mate search effort should decrease with the cost of sampling additional mates and increase with the number of possible ornaments that females can choose from. The potential for multiple exaggerated ornaments to coexist depends on subtleties of their cost structure: strict trade-offs (additive costs) favour sequential ornament evolution, whereas looser trade-offs (multiplicative costs) allow for coexistence. Lastly, we show that pleiotropy affecting both ornaments and preferences makes it difficult for Fisherian runaway to initiate, increasing the evolutionary time until ornamentation. Our model highlights the important but neglected role of mate search effort in sexual selection.     

From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila

Wolbachia are maternally inherited bacteria that commonly spread through host populations by causing cytoplasmic incompatibility, often expressed as reduced egg hatch when uninfected females mate with infected males. Infected females are frequently less fecund as a consequence of Wolbachia infection. However, theory predicts that because of maternal transmission, these "parasites" will tend to evolve towards a more mutualistic association with their hosts. Drosophila simulans in California provided the classic case of a Wolbachia infection spreading in nature. Cytoplasmic incompatibility allowed the infection to spread through individual populations within a few years and from southern to northern California (more than 700 km) within a decade, despite reducing the fecundity of infected females by 15%-20% under laboratory conditions. Here we show that the Wolbachia in California D. simulans have changed over the last 20 y so that infected females now exhibit an average 10% fecundity advantage over uninfected females in the laboratory. Our data suggest smaller but qualitatively similar changes in relative fecundity in nature and demonstrate that fecundity-increasing Wolbachia variants are currently polymorphic in natural populations.     

A preliminary study of vocal communication in wild long-tailed macaques (Macaca fascicularis). II. Potential of calls to regulate intragroup spacing

This study is a preliminary assessment of the potential of long-tailed macaque (Macaca fascicularis) calls to operate in systems of within-group spacing. Covariation in the rate of occurrence of calls with party spread, size, and activity among wild individuals of one group suggested that four classes of calls may function in intragroup spacing. Two of them are “clear” calls of long duration and pronounced frequency modulation. Calling rate increased with party spread for low- and high-frequency variants of these calls during resting and feeding respectively, suggesting possible utility in maintenance of spatial relations over moderately long distances. A third “harsh” call was negatively correlated with party spread during foraging and may thus function to increase dispersion among foraging individuals. Another harsh call with a tonal onset was unique among all calls in the vocal repertoire in being more frequently performed by lone, isolated individuals than by macaques accompanied by others, suggesting a possible function in reestablishing contact that has been severed. The functional significance of these calls with respect to their acoustic structures is discussed. Macaques that use calls to regulate intragroup spacing can control communication distance and direction by their choice of acoustically different vocalizations. This choice may be affected not only by varying environmental constraints on sound transmission, but also by social and ecological factors such as intragroup competition.     

The dynamics of plant invasions: a case study of three exotic goldenrod species (Solidago L.) in Europe

The patterns of spread of the three exotic species Solidago altissima L., S. gigantea Ait. and S. graminifolia (L.) Salisb. after their introduction to Europe were investigated, based on herbarium specimens and literature records. The spread was analysed by mapping the localities for each decade since 1850. Cumulative numbers of localities as well as numbers of occupied grid squares showed a continuous increase since 1850 for all three species. The slopes, however, were significantly different among the species. Solidago gigantea had the highest colonization rate, followed by S. altissima , and finally S. graminifolia . The latter showed only a slight increase in abundance over time. The increase in diameter of the range in central Europe was logistic for S. altissima and S. gigantea with a rapid increase between 1850 and 1880. The spread of the species in area and time over Europe showed no clear front; new localities at large distances were simultaneously colonized. A large part of the actual range of S. altissima and S. gigantea was already achieved about 1950. It is assumed that the spread of the species followed the hierarchical diffusion model with several independent foci from which the species began to spread. The data suggest that S. altissima and S. gigantea will successfully spread further, leading to an increase in abundance and area, while S. graminifolia seems to spread slowly.     

High Trans-ethnic Replicability of GWAS Results Implies Common Causal Variants

Genome-wide association studies (GWAS) have detected many disease associations. However, the reported variants tend to explain small fractions of risk, and there are doubts about issues such as the portability of findings over different ethnic groups or the relative roles of rare versus common variants in the genetic architecture of complex disease. Studying the degree of sharing of disease-associated variants across populations can help in solving these issues. We present a comprehensive survey of GWAS replicability across 28 diseases. Most loci and SNPs discovered in Europeans for these conditions have been extensively replicated using peoples of European and East Asian ancestry, while the replication with individuals of African ancestry is much less common. We found a strong and significant correlation of Odds Ratios across Europeans and East Asians, indicating that underlying causal variants are common and shared between the two ancestries. Moreover, SNPs that failed to replicate in East Asians map into genomic regions where Linkage Disequilibrium patterns differ significantly between populations. Finally, we observed that GWAS with larger sample sizes have detected variants with weaker effects rather than with lower frequencies. Our results indicate that most GWAS results are due to common variants. In addition, the sharing of disease alleles and the high correlation in their effect sizes suggest that most of the underlying causal variants are shared between Europeans and East Asians and that they tend to map close to the associated marker SNPs.     

Effects of active versus passive dendritic membranes on the transfer properties of a simulated neuron

In a simulated neuron with a dendritic tree, the relative effects of active and passive dendritic membranes on transfer properties were studied. The simulations were performed by means of a digital computer. The computations calculated the changes in transmembrane voltages of many compartments over time as a function of other biophysical variables. These variables were synaptic input intensity, critical firing threshold, rate of leakage of current across the membrane, and rate of longitudinal current spread between compartments. For both passive and active dendrites, the transfer properties of the soma studied for different rates of longitudinal current spread. With low rates of current spread, graded changes in firing threshold produced correspondingly graded changes in output discharge. With high rates of current spread, the neuron became a bistable operator where spiking was enhanced if the threshold was below a certain level and suppressed if the threshold was above that level. Since alterations in firing threshold were shown to have the same effect on firing rate as alterations in synaptic input intensity, the neuron can be said to change from graded to contrast-enhancing in its response to stimuli of different intensities. The presence or absence of dendritic spiking was found to have a significant effect on the integrative properties of the simulated neuron. In particular, contrast enhancement was considerably more pronounced in neurons with passive than with active dendrites in that somatic spike rates reached a higher maximum when dendrites were passive. With active dendrites, a less intense input was needed to initiate somatic spiking than with passive dendrites because a distal dendritic spike could easily propagate by means of longitudinal current spread to the soma. Once somatic spiking was initiated, though, spike rates tended to be lower with active than with passive dendrites because the soma recovered more slowly from its post-spike refractory period if it was also influenced by refractory periods in the dendrites. The experiment of comparing neurons with active and passive dendrites was repeated at a different, higher value of synaptic input. The same differences in transfer properties between the active and passive cases emerged as before. Spiking patterns in neurons with active dendrites were also affected by the time distribution of synaptic inputs. In a previous study, inputs had been random over both space and time, varying about a predetermined mean, whereas in the present study, inputs were random over space but uniform over time. When inputs were made uniform over time, spiking became more difficult to initiate and the transition from graded to bistable response became less sharp.     

Occupancy is nine-tenths of the law: occupancy rates determine the homogenizing and differentiating effects of exotic species

Biotic homogenization, the loss of local biotic distinctiveness among locations (beta diversity), is a form of global change that can result from the widespread introduction of non-native species. Here, we model this process using only species' occupancy rates--the proportion of sites they occupy--without reference to their spatial arrangement. The nonspatial model unifies many empirical results and reliably explains >90% of the variance in species' effects on beta diversity. It also provides new intuitions and principles, including the conditions under which species' appearance, spread, or extirpation will homogenize or differentiate landscapes. Specifically, the addition or spread of exotic species that are more common than the native background rate (effective occupancy) homogenizes landscapes, while driving such species to extinction regionally or introducing rarer species differentiates them. Given the primacy of occupancy and our model's ability to explain its role, homogenization research can now focus on other factors.     

Effects of dispersal on local population increase

Work to date on biological invasions and the spread of biological control agents has been focused on the explicitly spatial aspects, such as rate of spread and shape of the wave front. There has been relatively little attention paid to the influence of dispersal on the rate of increase of local populations. We use a simple general model for logistic local growth and one-dimensional diffusive dispersal to show that dispersal can act as a substantial drain on local populations. Local increase at a site of introduction is always slower than would be expected in the absence of dispersal, while the rate of increase of other populations is initially enhanced, then reduced by dispersal. This may have an important effect when estimating population parameters for invading organisms or biological control agents during the initial stages of their spread, and helps explain the "latent period" typically observed in biological invasions.     

The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina

Symbionts that distort their host''s sex ratio by favouring the production and survival of females are common in arthropods. Their presence produces intense Fisherian selection to return the sex ratio to parity, typified by the rapid spread of host ‘suppressor’ loci that restore male survival/development. In this study, we investigated the genomic impact of a selective event of this kind in the butterfly Hypolimnas bolina. Through linkage mapping, we first identified a genomic region that was necessary for males to survive Wolbachia-induced male-killing. We then investigated the genomic impact of the rapid spread of suppression, which converted the Samoan population of this butterfly from a 100∶1 female-biased sex ratio in 2001 to a 1∶1 sex ratio by 2006. Models of this process revealed the potential for a chromosome-wide effect. To measure the impact of this episode of selection directly, the pattern of genetic variation before and after the spread of suppression was compared. Changes in allele frequencies were observed over a 25 cM region surrounding the suppressor locus, with a reduction in overall diversity observed at loci that co-segregate with the suppressor. These changes exceeded those expected from drift and occurred alongside the generation of linkage disequilibrium. The presence of novel allelic variants in 2006 suggests that the suppressor was likely to have been introduced via immigration rather than through de novo mutation. In addition, further sampling in 2010 indicated that many of the introduced variants were lost or had declined in frequency since 2006. We hypothesize that this loss may have resulted from a period of purifying selection, removing deleterious material that introgressed during the initial sweep. Our observations of the impact of suppression of sex ratio distorting activity reveal a very wide genomic imprint, reflecting its status as one of the strongest selective forces in nature.     

SEXUAL SELECTION,SPACE, AND SPECIATION

A Fisherian model of sexual selection is combined with a diffusion model of mate dispersal to investigate the evolution of assortative mating in a sympatric population. Females mate with one of two types of polygynous males according to a male's display of one of two sex-limited, autosomal traits; these male traits may be associated with differential phenotypic mortalities. Through a Fisherian runaway process, female preferences and male traits can become associated in linkage disequilibrium, leading to patterns of assortative mating. Dispersing males, whose rate of movement is dependent on mating success, carry female preference genes with them, and displaced males thereby produce daughters with preference genes for their respective traits in locally higher than average frequencies. The reduced diffusion of the more preferred males permits the success of other male types in adjacent areas. Thus, mating-success dependent diffusion, when coupled with the rapid divergence in phenotypes possible under the Fisher process, can lead to the coexistence of two female preferences and two male traits in sympatry. We argue that many existing approaches to sympatric speciation fail to explain observed male polymorphisms because they exclude explicit spatial structure from their speciation models.     

Dynamics of biological invasions and pathways over time: a case study of a temperate coastal sea

Coastal and regional sea ecosystems suffer from several human-induced stressors, including human mediated bioinvasions. The Baltic Sea is generally considered to be susceptible to invasions by non-indigenous species (NIS). Out of the total of 132 NIS and cryptogenic species recorded, 59% are currently established in at least one country surrounding the Baltic Sea. On average, each country currently hosts 27 such species with 15% of the established species being found in at least 50% of the countries. Benthic macroinvertebrates dominate, both among those recorded (48%) and established (59%) species. Shipping, deliberate stocking and natural spread of NIS previously introduced to the North Sea are the main introduction pathways, with considerable dynamics over time. Amongst the pathways responsible for the currently established species, shipping and natural spread strongly dominate. Substantial uncertainty in the information on introduction pathways (except for deliberate releases) hampers detailed analyses and poses major challenges for management. Spatio-temporal variability in the invasion dynamics reflects both the spatial differences in the main hydrographic conditions of the Baltic Sea as well as the availability of introduction pathways. We conclude that the Baltic Sea cannot be considered as a uniform waterbody in terms of the established introduced species and at least two major regions with differing hydrographic conditions and introduction pathways can be clearly distinguished. Due to the importance of natural spread of NIS from the North Sea, regional cooperation in bioinvasion management should be enhanced in the future.     

Clustered or scattered? The impact of habitat quality clustering on establishment and early spread

The match between the environmental conditions of an introduction area and the preferences of an introduced species is the first prerequisite for establishment. Yet, introduction areas are usually landscapes, i.e. heterogeneous sets of habitats that are more or less favourable to the introduced species. Because individuals are able to disperse after their introduction, the quality of the habitat surrounding the introduction site is as critical to the persistence of introduced populations as the quality of the introduction site itself. Moreover, demographic mechanisms such as Allee effects or dispersal mortality can hamper dispersal and affect spread across the landscape, in interaction with the spatial distribution of favourable habitat patches. In this study, we investigate the impact of the spatial distribution of heterogeneous quality habitats on establishment and early spread. First, we simulated introductions in one‐dimensional landscapes for different dispersal rates and either dispersal mortality or Allee effects. The landscapes differed by the distribution of favourable and less favourable habitats, which were either clustered into few large aggregates of the same quality or scattered into multiple smaller ones. Second, we tested the predictions of simulations by performing experimental introductions of hymenopteran parasitoids (Trichogramma chilonis) in ‘clustered’ and ‘scattered’ microcosm landscapes. Results highlighted two impacts of the clustering of favourable habitat: by decreasing the risks of dispersal from the introduction site to unfavourable habitat early during the invasion, it increased establishment success. However, by increasing the distance between favourable habitat patches, it also hindered the subsequent spread of introduced species over larger areas.     

The polymorphism architecture of mouse genetic resources elucidated using genome-wide resequencing data: implications for QTL discovery and systems genetics

Mouse genetic resources include inbred strains, recombinant inbred lines, chromosome substitution strains, heterogeneous stocks, and the Collaborative Cross (CC). These resources were generated through various breeding designs that potentially produce different genetic architectures, including the level of diversity represented, the spatial distribution of the variation, and the allele frequencies within the resource. By combining sequencing data for 16 inbred strains and the recorded history of related strains, the architecture of genetic variation in mouse resources was determined. The most commonly used resources harbor only a fraction of the genetic diversity of Mus musculus, which is not uniformly distributed thus resulting in many blind spots. Only resources that include wild-derived inbred strains from subspecies other than M. m. domesticus have no blind spots and a uniform distribution of the variation. Unlike other resources that are primarily suited for gene discovery, the CC is the only resource that can support genome-wide network analysis, which is the foundation of systems genetics. The CC captures significantly more genetic diversity with no blind spots and has a more uniform distribution of the variation than all other resources. Furthermore, the distribution of allele frequencies in the CC resembles that seen in natural populations like humans in which many variants are found at low frequencies and only a minority of variants are common. We conclude that the CC represents a dramatic improvement over existing genetic resources for mammalian systems biology applications.     

Meta-analysis suggests choosy females get sexy sons more than "good genes"

Female preferences for specific male phenotypes have been documented across a wide range of animal taxa, including numerous species where males contribute only gametes to offspring production. Yet, selective pressures maintaining such preferences are among the major unknowns of evolutionary biology. Theoretical studies suggest that preferences can evolve if they confer genetic benefits in terms of increased attractiveness of sons ("Fisherian" models) or overall fitness of offspring ("good genes" models). These two types of models predict, respectively, that male attractiveness is heritable and genetically correlated with fitness. In this meta-analysis, we draw general conclusions from over two decades worth of empirical studies testing these predictions (90 studies on 55 species in total). We found evidence for heritability of male attractiveness. However, attractiveness showed no association with traits directly associated with fitness (life-history traits). Interestingly, it did show a positive correlation with physiological traits, which include immunocompetence and condition. In conclusion, our results support "Fisherian" models of preference evolution, while providing equivocal evidence for "good genes." We pinpoint research directions that should stimulate progress in our understanding of the evolution of female choice.     

Cultural coevolution of norm adoption and enforcement when punishers are rewarded or non-punishers are punished

A number of studies have shown that social norms can be maintained at a high frequency when norm-violators are punished. However, there remains the problem of how norm-adopters and punishers coevolve within a single group. We develop a recursive system to examine the coevolution of norm-adopters and punishers where the viability of punishers is enhanced by one of two "metanorms": (1) Norm-observers reward punishers for punishing norm-violators (Reward Model); (2) Punishers punish non-punishers (Punishment Model). Both models generate a bistable system and each is characterized in phenotype frequency space by a distinct region of attraction to the equilibrium consisting of only norm-adopting punishers. Using a Monte Carlo simulation, we find that cultural drift may allow norm-adopters and punishers to coevolve from invasion into this region of attraction, resulting in their fixation. This coevolution typically occurs across a wider range of conditions under the reward- than the punishment-based metanorm. We also show that, under appropriate conditions, a large negative statistical association between the two traits may evolve only under the Reward Model. Furthermore, for each metanorm, a population of norm-adopters who always observe the norm can be locally stable over a continuum of punishment frequencies.     

DYNAMICS OF SEXUAL SELECTION IN DIPLOID POPULATIONS

We describe results for a diploid, two-locus model for the evolution of a female mating preference directed at an attractive male trait that is subject to viability and/or fertility selection. Using computer simulation, we studied a large, random sample of parameter values, assuming additivity of alleles at the preference locus and partial dominance at the trait locus. Simulation results were classifiable into nine types of parameter sets, each differing in equilibria, evolutionary trajectories, and rates of evolution. For many parameters, evolutionary trajectories converged on curves within the allelic frequency plane and subsequently evolved along the curves toward fixation. Neutrally stable curves of equilibria did not occur in Fisherian models that assume only viability and sexual selection unless there is complete dominance at the trait locus. The Fisherian models also exhibited oscillation of allelic frequencies and unique polymorphic equilibria. “Sexy son” models in which attractive males had reduced fertility were much less likely to lead to increase in traits and preferences than were the Fisherian models. However, if less fertile males had increased viability, trait polymorphisms and fixation of rare “sexy” alleles occurred. In general, the behavior of the diploid model was much more complex than that of analogous haploid or polygenic models.     

Spatial dynamics of adaptive sex ratios

According to Fisherian sex allocation theory, parents that can adjust their offspring sex ratio in response to skews in population sex ratio will maximize their fitness over parents lacking this ability. There is good evidence that adaptive sex ratio adjustment occurs in many natural populations, but deviations from theoretical predictions have also been observed. These anomalies may be more apparent than real. When the spatial dimension of sex ratio variation is ignored, then a mismatch between empirical data and theoretical predictions based on panmictic mating is to be expected. We illustrate this with data on human sex ratio variation in 21 preindustrial populations, and with a cellular automaton model built to obey Fisherian sex allocation rules. The results from the model generally match with the data. When information about the ambient sex ratio is limited, then the sex allocation decisions may appear locally maladaptive. In general, the results indicate that Fisher's sex-ratio theory may have greater explanatory power than previously thought.