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PubMed2004

Adaptation varies through space and time in a coevolving host-parasitoid interaction.

One of the central challenges of evolutionary biology is to understand how coevolution organizes biodiversity over complex geographic landscapes. Most species are collections of genetically differentiated populations, and these populations have the potential to become adapted to their local environments in different ways. The geographic mosaic theory of coevolution incorporates this idea by proposing that spatial variation in natural selection and gene flow across a landscape can shape local coevolutionary dynamics. These effects may be particularly strong when populations differ across productivity gradients, where gene flow will often be asymmetric among populations. Conclusive empirical tests of this theory have been particularly difficult to perform because they require knowledge of patterns of gene flow, historical population relationships and local selection pressures. We have tested these predictions empirically using a model community of bacteria and bacteriophage (viral parasitoids of bacteria). We show that gene flow across a spatially structured landscape alters coevolution of parasitoids and their hosts and that the resulting patterns of adaptation can fluctuate in both space and time.

Adaptation, Physiological↗

PubMed2003

Synchronous coadaptation in an ancient case of herbivory.

Coevolution has long been considered a major force leading to the adaptive radiation and diversification of insects and plants. A fundamental aspect of coevolution is that adaptations and counteradaptations interlace in time. A discordant origin of traits long before or after the origin of the putative coevolutionary selective pressure must be attributed to other evolutionary processes. Despite the importance of this distinction to our understanding of coevolution, the macroevolutionary tempo of innovation in plant defenses and insect counterdefenses has not been documented. Molecular clocks for a lineage of chrysomelid beetles of the genus Blepharida and their Burseraceae hosts were independently calibrated. Results show that these plants' defenses and the insect's counterdefensive feeding traits evolved roughly in synchrony, providing macroevolutionary confirmation of synchronous plant-herbivore coadaptation. The association between these two groups of organisms was determined to be about 112 million years old, the oldest age so far for a specialized plant-herbivore association.

Adaptation, Physiological↗

PubMed2006

Phylogenetic methodology for detecting protein interactions.

Detecting protein-protein interactions and assigning proteins to functional complexes are key challenges of modern biology. The rise of genomics has lead to evidence that correlated patterns of presence/absence and/or fusing of proteins in any organism suggest these proteins interact. Unfortunately, methods based on such data work best with divergent genomes, whereas major sequencing efforts in vertebrates, for example, are yielding alignments of the same set of proteins sampled from the same set of taxa (species). Using vertebrate mitochondrial genomes to illustrate a novel method, we associate proteins based on vectors of their evolutionary tree edge (branch or internode) lengths. This approach is based on the expectation that molecular coevolution is greatest between proteins that interact in some way. Mitochondrial DNA-encoded proteins are associated into groups largely consistent with the complexes they come from. This association is apparently not due to the tree structure or mutation processes, leaving coevolution as the best explanation. We show that it is important that the tree used to derive the edge-length vector is estimated accurately in terms of both topology and edge lengths. Although more complex substitution models reduce systematic error, they also inflate stochastic error. This makes the use of less complex substitution models preferable in some circumstances. We describe a method to estimate correlations of pairwise evolutionary distances, which adjusts for non-independent correlations due to shared evolutionary history. Associations of proteins based on their edge-length vectors are visualized and assessed using a variety of hierarchical clustering and multidimensional scaling methods. New formula for estimating the fit of data to model, including the average percent standard deviation of distances on least squares trees, are presented. Use of edge-length vectors is compared and contrasted with correlated distance methods, correlated rates methods, and site-specific evidence of coevolution.

Cluster Analysis↗

PubMed1993

Phylogenetic analysis of the outer-membrane-protein genes of Chlamydiae, and its implication for vaccine development.

Examination of 18 complete and 6 partial sequences of the major outer-membrane protein from 24 chlamydiae isolates was used to reconstruct their evolutionary relationships. From this analysis, assuming that the clades with 100% bootstrap support are correct, come the following conclusions: (1) The tree of these sequences is not congruent with the phylogeny of the hosts, and thus host switching would seem to have occurred, thereby limiting the extent to which there has been coevolution of parasite and host. (2) The tree is also noncongruent with clustering by type of cell infected, thereby limiting the extent to which there has been coevolution of parasite and the cell type that it infects. (3) The tree is also noncongruent with clustering by the organ infected (eyes or genitalia), thereby limiting the extent to which there has been coevolution of parasite and the organ that it infects. (4) The tree is also noncongruent with genital strains arising from lymphogranuloma venereum strains. (5) The tree is also noncongruent with the geographic site at which the isolates were obtained, thereby limiting the extent of divergence explained by geographic separation. (6) There are estimated to be 185 amino acid positions that are invariable (as opposed to unvaried) in the major outer-membrane protein. There are 10 unvaried positions in the variable domains, of which 9 appear to be invariable, giving some reason to hope that development of a vaccine might be possible. (7) The rate of change of this protein is too small to see increased divergence over the time span of isolation of these genes, giving hope to any vaccine having longevity. Bootstrapping supports those portions of the tree on which the first five conclusions above depend. The picture that these results provide is more one of pathogen versatility than one of coevolutionary constraints. In addition, we examined 10 60-KDa, outer-membrane protein-2 genes, all but one of which were from these same strains. The tree was not, among the trachomatis strains, congruent with the major-outer-membrane protein tree, suggesting that gene exchange could be occurring among strains. Moreover, there is an apparent slowdown in divergence in this gene, among the trachomatis strains.

Amino Acid Sequence↗

PubMed2001

Evolution of female remating behaviour following experimental removal of sexual selection.

The relatively small number of ova produced by a female can be fertilized by a single ejaculate in most species. Why females of many species mate with multiple males is therefore enigmatic, especially given that costs associated with remating have been well documented. Recently, it has been argued that females may remate at a maladaptive rate as an outcome of sexually antagonistic coevolution: the evolutionary tug-of-war between manipulation by one sex and resistance to being manipulated by the other sex. We tested this hypothesis experimentally for the evolution of the female remating interval in a naturally promiscuous species, Drosophila melanogaster. In two replicate populations, sexual selection was removed through enforced monogamous mating with random mate assignment, or retained in polyandrous controls. Monogamy constrains the reproductive success of mates to be identical, thereby converting prior conflicts between mates into opportunities for mutualism. Under these experimental conditions, the sexually antagonistic coevolution hypothesis generates explicit predictions regarding the direction of evolutionary change in female remating behaviour. These predictions are contingent upon the mechanism of male manipulation, which may be mediated biochemically by seminal fluids or behaviourally by courtship. Levels of divergence in female remating interval across lines, and in male ejaculatory and courtship effects on female remating, were quantified after 84 generations of selection. Data refute the hypothesis that the evolutionary change in female remating behaviour was due to sexually antagonistic coevolution of courtship signal and receiver traits. The data were, however, consistent with a hypothesis of sexual conflict mediated through ejaculate manipulation. Monogamy-line males evolved ejaculates that were less effective in inducing female non-receptivity and monogamy-line females evolved to remate less frequently, symptomatic of lowered resistance to ejaculate manipulation. The consistency of the results with alternative hypotheses to explain female promiscuity are discussed.

Animals↗

PubMed2002

Heteropopulation males have a fertilization advantage during sperm competition in the yellow dung fly (Scathophaga stercoraria).

Sexual conflict occurs whenever there is not strict genetic monogamy. The sexually antagonistic coevolution that potentially occurs because of this conflict involves adaptation by one sex followed by the counter-adaptation by the other, and may be thought of as an evolutionary arms-race. As a result of these cycles of antagonistic coevolution, females from one population may be less resistant to heteropopulation males, at least after short periods of allopatry, as they will not have evolved any resistance to them. We tested this prediction in yellow dung fly (Scathophaga stercoraria) populations from the UK and Switzerland. Males from each population mated as first and second males to females from each population, and the mean numbers of offspring sired by the last male to mate in each situation were compared. We also compared the fertility and fecundity of single females mated to males from both populations, as well as the fertility and fecundity of the F(1) crosses. Both crosses produced viable and fertile offspring and the offspring sex ratios were not skewed. However, the fecundity of F(1)-cross females was greater than that of the parentals. In the sperm-competition experiment, there was a significant interaction between male and female origin influencing the proportion of offspring sired by the second male to mate, with heteropopulation males always outcompeting conpopulation males. This effect was independent of copula duration and the delay between copulations. In a separate experiment, we tested to see whether this was due to female preference for genetically dissimilar males but found no evidence for paternity biasing based on genetic similarity. Our results therefore seem to be best explained by sexually antagonistic coevolution as females appear less resistant to males with which they have not coevolved.

Adaptation, Physiological↗

PubMed2005

Cadherins in maternal-foetal interactions: red queen with a green beard?

Cadherins are homophilic cell surface adhesion proteins, some of which mediate interactions between maternal and foetal tissues during mammalian pregnancy. David Haig suggested that these proteins may exhibit 'green-beard gene' effects, whereby the nature of binding between identical alleles in mother and foetus leads to differential levels of resource transfer. The selfish effects of such self-recognizing alleles should, however, be suppressed over evolutionary time by unlinked genes, which is expected to lead to antagonistic coevolution between placentally expressed cadherins and unlinked modifiers. Such molecular coevolution should leave a signature of positive selection, with high ratios of non-synonymous to synonymous amino acid substitution. We present evidence that three placentally expressed cadherin genes, E-cadherin, P-cadherin and VE-cadherin, have been subject to positive selection. By contrast, a 'control' cadherin that is not expressed in the placenta, H-cadherin, showed no evidence of selection. These results provide support for the hypothesis that the cadherin genes involved in maternal-foetal interactions have been subject to green-beard-effect mutations over the course of evolutionary history, leading to antagonistic coevolution with suppressing elements from the parliament of genes.

Animals↗

PubMed2006

Quantifying the gender load: can population crosses reveal interlocus sexual conflict?

Six sister populations of Drosophila melanogaster kept under identical environmental conditions for greater than 600 generations were reciprocally crossed to investigate the incidence of population divergence in allopatry. Population crosses directly influenced fitness, mating frequency, and sperm competition patterns. Changes in both female remating rate and the outcome of male sperm competition (P1, P2) in response to foreign males were consistent with intersexual coevolution. Moreover, seven of the 30 crosses between foreign mates resulted in significant reductions in female fitness, whereas two resulted in significant increases, compared to local matings. This tendency for foreign males to reduce female fitness may be interpreted as evidence for either sexually antagonistic coevolution or the disruption of mutualistic interactions. However, instances in which female fitness improved via cohabitation with foreign males may better reveal sexual conflict, signalling release from the cost of interacting with locally adapted males. By this metric, female reproduction in D. melanogaster is strongly constrained by local adaptation by males, a situation that would promote antagonistic coevolution between the sexes. We conclude that sexual selection can promote population differentiation in allopatry and that sexual conflict is likely to have played a role in population differentiation in this study system.

Animals↗

PubMed2006

Sensory exploitation and sexual conflict.

Much of the literature on male-female coevolution concerns the processes by which male traits and female preferences for these can coevolve and be maintained by selection. There has been less explicit focus on the origin of male traits and female preferences. Here, I argue that it is important to distinguish origin from subsequent coevolution and that insights into the origin can help us appreciate the relative roles of various coevolutionary processes for the evolution of diversity in sexual dimorphism. I delineate four distinct scenarios for the origin of male traits and female preferences that build on past contributions, two of which are based on pre-existing variation in quality indicators among males and two on exploitation of pre-existing sensory biases among females. Recent empirical research, and theoretical models, suggest that origin by sensory exploitation has been widespread. I argue that this points to a key, but perhaps transient, role for sexually antagonistic coevolution (SAC) in the subsequent evolutionary elaboration of sexual traits, because (i) sensory exploitation is often likely to be initially costly for individuals of the exploited sex and (ii) the subsequent evolution of resistance to sensory exploitation should often be associated with costs due to selective constraints. A review of a few case studies is used to illustrate these points. Empirical data directly relevant to the costs of being sensory exploited and the costs of evolving resistance is largely lacking, and I stress that such data would help determining the general importance of sexual conflict and SAC for the evolution of sexual dimorphism.

Animals↗

PubMed2006

The evolutionary outcome of sexual conflict.

Inter-locus sexual conflict occurs by definition when there is sexually antagonistic selection on a trait so that the optimal trait value differs between the sexes. As a result, there is selection on each sex to manipulate the trait towards its own optimum and resist such manipulation by the other sex. Sexual conflict often leads additionally to the evolution of harmful behaviour and to self-reinforcing and even perpetual sexually antagonistic coevolution. In an attempt to understand the determinants of these different outcomes, I compare two groups of traits-those related to parental investment (PI) and to mating-over which there is sexual conflict, but which have to date been explored by largely separate research traditions. A brief review suggests that sexual conflict over PI, particularly over PI per offspring, leads less frequently to the evolution of manipulative behaviour, and rarely to the evolution of harmful behaviour or to the rapid evolutionary changes which may be symptomatic of sexually antagonistic coevolution. The chief determinants of the evolutionary outcome of sexual conflict are the benefits of manipulation and resistance, the costs of manipulation and resistance, and the feasibility of manipulation. All three of these appear to contribute to the differences in the evolutionary outcome of conflicts over PI and mating. A detailed dissection of the evolutionary changes following from sexual conflict exposes greater complexity than a simple adaptation-counter-adaptation cycle and clarifies the role of harm. Not all of the evolutionary changes that follow from sexual conflict are sexually antagonistic, and harm is not necessary for sexually antagonistic coevolution to occur. In particular, whereas selection on the trait over which there is conflict is by definition sexually antagonistic, collateral harm is usually in the interest of neither sex. This creates the opportunity for palliative adaptations which reduce collateral harm. Failure to recognize that such adaptations are in the interest of both sexes can hinder our understanding of the evolutionary outcome of sexual conflict.

Animals↗

PubMed2006

Relative number of generations of hosts and parasites does not influence parasite local adaptation in coevolving populations of bacteria and phages.

A potential consequence of host-parasite coevolution in spatially structured populations is parasite local adaptation: local parasites perform better than foreign parasites on their local host populations. It has been suggested that the generally shorter generation times of parasites compared with their hosts contributes to parasites, rather than hosts, being locally adapted. We tested the hypothesis that relative generation times of hosts and parasites affect local adaptation of hosts and parasites, using the bacterium Pseudomonas fluorescens and a lytic phage as host and parasite, respectively. Generation times were not directly manipulated, but instead one of the coevolving partners was regularly removed and replaced with a population from an earlier time point. Thus, one partner underwent more generations than the other. Manipulations were carried out at both early and later periods of coevolutionary interactions. At early stages of coevolution, host and parasites that underwent relatively more generations displayed higher levels of resistance and infectivity, respectively. However, the relative number of generations that bacteria and phages underwent did not change the level of local adaptation relative to control populations. This is likely because generalist hosts and parasites are favoured during early stages of coevolution, preventing local adaptation. By contrast, at later stages manipulations had no effect on either average levels of resistance or infectivity, or alter the level of local adaptation relative to the controls, possibly because traits other than resistance and infectivity were under strong selection. Taken together, these data suggest that the relative generation times of hosts and parasites may not be an important determinant of local adaptation in this system.

Adaptation, Biological↗

PubMed2005

The coevolutionary dynamics of antagonistic interactions mediated by quantitative traits with evolving variances.

Quantitative traits frequently mediate coevolutionary interactions between predator and prey or parasite and host. Previous efforts to understand and predict the coevolutionary dynamics of these interactions have generally assumed that standing genetic variation is fixed or absent altogether. We develop a genetically explicit model of coevolution that bridges the gap between these approaches by allowing genetic variation itself to evolve. Analysis of this model shows that the evolution of genetic variance has important consequences for the dynamics and outcome of coevolution. Of particular importance is our demonstration that coevolutionary cycles can emerge in the absence of stabilizing selection, an outcome not possible in previous models of coevolution mediated by quantitative traits. Whether coevolutionary cycles evolve depends upon the strength of selection, the number of loci, and the rate of mutation in each of the interacting species. Our results also generate novel predictions for the expected sign and magnitude of linkage disequilibria in each species.

Biological Evolution↗

PubMed2006

Parasite local adaptation in a geographic mosaic.

A central prediction of the geographic mosaic theory of coevolution is that coevolving interspecific interactions will show varying degrees of local maladaptation. According to the theory, much of this local maladaptation is driven by selection mosaics and spatially intermingled coevolutionary hot and cold spots, rather than a simple balance between gene flow and selection. Here I develop a genetic model of host-parasite coevolution that is sufficiently general to incorporate selection mosaics, coevolutionary hot and cold spots, and a diverse array of genetic systems of infection/resistance. Results from this model show that the selection mosaics experienced by the interacting species are an important determinant of the sign and magnitude of local maladaptation. In some cases, this effect may be stronger than a previously described effect of relative rates of parasite and host gene flow. These results provide the first theoretical evidence that selection mosaics and coevolutionary hot and cold spots per se determine the magnitude and sign of local maladaptation. At the same time, however, these results demonstrate that coevolution in a geographic mosaic can lead to virtually any pattern of local adaptation or local maladaptation. Consequently, empirical studies that describe only patterns of local adaptation or maladaptation do not provide evidence either for or against the theory.

Adaptation, Physiological↗

PubMed1999

Reciprocal Natural Selection on Host-Parasite Phenotypes.

Coevolution is evolution in one species in response to selection imposed by a second species, followed by evolution in the second species in response to reciprocal selection imposed by the first species. Although reciprocal selection is a prerequisite of coevolution, it has seldom been documented in natural populations. We examined the feasibility of reciprocal selection in a simple host-parasite system consisting of feral pigeons (Columba livia) and their Ischnoceran feather lice (Phthiraptera: Insecta). We tested for a selective effect of parasites on hosts with experimentally altered defenses and for a selective effect of host defense on a component of parasite escape. Previous work indicates that pigeons control lice through efficient preening, while lice escape from preening using complex avoidance behavior. Our results show that feral pigeons with impaired preening, owing to slight bill deformities, have higher louse loads than pigeons with normal bills. We use a controlled experiment to show that high louse loads reduce the survival of pigeons, suggesting that lice select for efficient preening and against bill deformities. In a reciprocal experiment, we demonstrate that preening with a normal bill selects for small body size in lice, which may facilitate their escape from preening. The results of this study verify a crucial element of coevolutionary theory by identifying likely targets of reciprocal phenotypic selection between host and parasite.

birds↗

PubMed2026

Disruption of mitonuclear coadaptation and compensatory evolution after an extreme dietary shift in carnivorous butterflies.

Mitochondrial function depends on tight coordination between mitochondrial and nuclear genomes, which requires long-term coevolution to maintain mitonuclear coadaptation. While mitonuclear incompatibility is typically studied in the context of hybridization, other evolutionary scenarios that may disrupt coadaptation between the two genomes remain less explored. Here, we propose that extreme ecological niche shifts may disrupt mitonuclear coadaptation, which we test in carnivorous Miletinae butterflies with an extreme dietary transition. By generating high-quality genome assemblies, we found that Miletinae exhibit extensive chromosomal rearrangements. Comparative phylogenomic analyses revealed a striking asymmetric mitonuclear evolutionary response: Miletinae exhibit elevated mitochondrial nucleotide substitution rates compared to phytophagous relatives, whereas nuclear rates remain stable. This shift reverses the typical lepidopteran pattern where nuclear rates exceed mitochondrial rates. Interestingly, this mitochondrial acceleration is driven primarily by relaxed purifying selection rather than positive selection. To sustain mitochondrial function, the nuclear genome of Miletinae underwent pervasive, multilayered compensatory evolution. We detected strong signatures of positive selection and accelerated evolution in nuclear genes directly interacting with mitochondrial components across oxidative phosphorylation (OXPHOS) complexes, the mitochondrial translation, and replication and transcription machinery. Furthermore, this nuclear compensatory response extends to systems governing mitochondrial homeostasis, including protein quality control and RNA degradation and stabilization. Our results support a model in which extreme ecological transitions can disrupt ancestral mitonuclear coadaptation and promote the emergence of a new coadapted state through systemic nuclear compensation. This study broadens the conceptual framework of mitonuclear coevolution and highlights its role in facilitating evolutionary persistence after major ecological shifts.

Animals↗

PubMed1984

Insect--plant adaptations.

The adaptation of insects to plants probably commenced in the early Permian period, though most current associations will be more recent. A major burst of adaptation must have followed the rise of the Angiosperms in the Cretaceous period, though some particular associations are as recent as this century. Living plants form a large proportion of the potential food in most habitats, though insects have had to overcome certain general hurdles to live and feed on them. Insects affect the reproduction and survival of plants, and thus the diversity of plant secondary chemicals may have evolved as a response. Where an insect species has a significant effect on a plant species that is its only host, coevolution may be envisaged. A spectacular example is provided by Heliconius butterflies and passion flower vines, studied by L.E. Gilbert and others. But such cases may be likened to 'vortices in the evolutionary stream': most plant species are influenced by a range of phytophagous insects so that selection will be for general defences--a situation termed diffuse coevolution. Evidence is presented on recent host-plant shifts to illustrate both the restrictions and the flexibility in current insect-plant associations.

Adaptation, Biological↗

PubMed2005

Cooperative evolution in protein complexes of yeast from comparative analyses of its interaction network.

A comparative analysis among Saccharomyces cerevisiae and the other four yeasts Candida glabrata, Kluyveromyces lactis, Debaryomyces hansenii, and Yarrowia lipolytica is presented. The broad evolutionary range spanned by the organisms allows to quantitatively demonstrate novel evolutionary effects in protein complexes. The evolution rates within cliques of interlinked proteins are found to bear strong multipoint correlations, witnessing a cooperative coevolution of complex subunits. The coevolution is found to be largely independent of the tendency of the subunits to have similar abundances.

Candida glabrata↗

PubMed1999

Female responses to isolated signals from multimodal male courtship displays in the wolf spider genus Schizocosa (Araneae: Lycosidae).

Male wolf spiders within the genus Schizocosa display considerable variation in foreleg ornamentation as well as in courtship communication. Multiple modes of male signalling have evolved in a number of species. Divergence in courtship signals among species within this genus may be directly associated with variation in the sensory sensitivities of conspecific females. We isolated the visual and vibratory courtship cues of four species of Schizocosa and recorded conspecific female receptivity to each isolated cue. We also examined female receptivity to complete multimodal courtship signals. We found that the sensory sensitivities of conspecific females were associated with the predominant modes of male courtship communication. Species in which females use mostly stridulatory cues in assessing conspecific males tended to have stridulation-based male courtship displays (S. duplex and S. uetzi) while the opposite was true for species in which females used more visual cues in male assessment (S. stridulans and S. crassipes). This study suggests coevolution between male signal design and female sensory design. We discuss possible scenarios that could be driving this coevolution, including hypotheses of sensory bias and environmental constraints. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗