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Host-parasite relationships among bolete infecting Hypomyces species.

Host specificity of the mycoparasite Hypomyces microspermus to the Xerocomus chrysenteron group has been observed, but primarily from European collections. Our objectives were to test host specificity among Hypomyces spp. associated with boletes in California oak-woodlands, investigate population biology of these parasites, and to initiate studies on host-parasite coevolution. Bolete samples were collected from four locations separated by up to 600 km. Hypomyces isolates were cultured and host tissue samples taken for molecular identification. Based on AFLP analysis, four distinct Hypomyces clades were found with little genotypic diversity within each group. ITS-rDNA regions of selected isolates from each group were sequenced and analyzed along with sequences from a previously published phylogeny. Isolates from two AFLP groups clustered with H. microspermus whereas isolates from the other two AFLP groups clustered with H. chrysospermus. ITS-RFLP followed by sequence analysis identified three bolete hosts: (1) X. dryophilus; (2) a Xerocomus species closely related to X. dryophilus with affinities to X. chrysenteron; and (3) a Xerocomus species related to the X. subtomentosus group, which is not closely related to X. dryophilus and X. chrysenteron. H. microspermus infected X. dryophilus and the species with affinities to X. chrysenteron, whereas H. chrysospermus infected the species with affinities to X. chrysenteron and the species related to the X. subtomentosus group. These results support previous observations that H. microspermus is host-specific to the X. chriysenteron group, and that H. chrysospermus is more of a generalist pathogen. We also conclude that host-parasite coevolution studies within this system will not be possible until a phylogeny of North American boletes is in place.

Basidiomycota↗

The coevolutionary dynamics of obligate ant social parasite systems--between prudence and antagonism.

In this synthesis we apply coevolutionary models to the interactions between socially parasitic ants and their hosts. Obligate social parasite systems are ideal models for coevolution, because the close phylogenetic relationship between these parasites and their hosts results in similar evolutionary potentials, thus making mutual adaptations in a stepwise fashion especially likely to occur. The evolutionary dynamics of host-parasite interactions are influenced by a number of parameters, for example the parasite's transmission mode and rate, the genetic structure of host and parasite populations, the antagonists' migration rates, and the degree of mutual specialisation. For the three types of obligate ant social parasites, queen-tolerant and queen-intolerant inquilines and slavemakers, several of these parameters, and thus the evolutionary trajectory, are likely to differ. Because of the fundamental differences in lifestyle between these social parasite systems, coevolution should further select for different traits in the parasites and their hosts. Queen-tolerant inquilines are true parasites that exert a low selection pressure on their host, because of their rarity and the fact that they do not conduct slave raids to replenish their labour force. Due to their high degree of specialisation and the potential for vertical transmission, coevolutionary theory would predict interactions between these workerless parasites and their hosts to become even more benign over time. Queen-intolerant inquilines that kill the host queen during colony take-over are best described as parasitoids, and their reproductive success is limited by the existing worker force of the invaded host nest. These parasites should therefore evolve strategies to best exploit this fixed resource. Slavemaking ants, by contrast, act as parasites only during colony foundation, while their frequent slave raids follow a predator prey dynamic. They often exploit a number of host species at a given site, and theory predicts that their associations are best described in terms of a highly antagonistic coevolutionary arms race.

Animals↗

Positive selection in the evolution of cancer.

We hypothesize that forms of antagonistic coevolution have forged strong links between positive selection at the molecular level and increased cancer risk. By this hypothesis, evolutionary conflict between males and females, mothers and foetuses, hosts and parasites, and other parties with divergent fitness interests has led to rapid evolution of genetic systems involved in control over fertilization and cellular resources. The genes involved in such systems promote cancer risk as a secondary effect of their roles in antagonistic coevolution, which generates evolutionary disequilibrium and maladaptation. Evidence from two sources: (1) studies on specific genes, including SPANX cancer/testis antigen genes, several Y-linked genes, the pem homebox gene, centromeric histone genes, the breast cancer gene BRCA1, the angiogenesis gene ANG, cadherin genes, cytochrome P450 genes, and viral oncogenes; and (2) large-scale database studies of selection on different functional categories of genes, supports our hypothesis. These results have important implications for understanding the evolutionary underpinnings of cancer and the dynamics of antagonistically-coevolving molecular systems.

Animals↗

Phylogeography of sex ratio and multiple mating in stalk-eyed flies from southeast Asia.

The factors maintaining sex chromosome meiotic drive, or sex ratio (SR), in natural populations remain uncertain. Coevolution between segregation distortion and modifiers should produce transient SR distortion while selection can result in a stable polymorphism. We hypothesize that if SR is maintained by selection, then phylogenetically related populations should exhibit similar SR frequency and intensity. Furthermore, when drive is present, females should mate with multiple males more often both to insure fertility and to increase the probability of producing male progeny. In this paper we report on variation in SR frequency and multiple mating among seven populations and three species of stalk-eyed flies, genus Cyrtodiopsis, from southeast Asia. Using a phylogenetic hypothesis based on 1100 bp of mtDNA sequence we find that while sex chromosome meiotic drive is present in all populations of C. whitei and C. dalmanni, the frequency and intensity of drive only differs between populations or species with greater than 4.8% sequence divergence. The frequency of females mating with multiple males is higher in populations with SR. In addition, SR males mate less often, possibly to compensate for sperm depletion. Our results suggest that sex chromosome drive is maintained by balancing selection in populations of C. whitei and C. dalmanni. Nevertheless, coevolution between drive and suppressors deserves further study.

Animals↗

Geographic structure and dynamics of coevolutionary selection.

Coevolution of species is one of the major processes organizing the Earth's biodiversity. Recent coevolutionary theory has indicated that the geographic structure of species has the potential to impose powerful and continuing effects on coevolutionary dynamics, if that structure creates selection mosaics and coevolutionary hotspots across landscapes. Here we confirm that current coevolutionary selection in interspecific interactions can be highly divergent across both narrow and broad geographic scales, thereby fueling continuing coevolution of taxa. Study of a widespread plant insect interaction across a broad range of habitats for several years showed that an insect functioning both as a pollinator and a floral parasite can be strongly mutualistic in some habitats but commensal or antagonistic in neighbouring habitats. The results for one of the habitats span seven years, demonstrating that the local structure of coevolutionary selection can remain stable across multiple generations. Conservation of the evolutionary processes maintaining long-term biological diversity may require preservation of the conditions that allow a long-term shifting geographic mosaic of coevolutionary hotspots and coldspots.

Animals↗

Testing a biosynthetic theory of the genetic code: fact or artifact?

It has long been conjectured that the canonical genetic code evolved from a simpler primordial form that encoded fewer amino acids [e.g., Crick, F. H. C. (1968) J. Mol. Biol. 38, 367-379]. The most influential form of this idea, "code coevolution" [Wong, J. T.-F. (1975) Proc. Natl. Acad. Sci. USA 72, 1909-1912], proposes that the genetic code coevolved with the invention of biosynthetic pathways for new amino acids. It further proposes that a comparison of modern codon assignments with the conserved metabolic pathways of amino acid biosynthesis can inform us about this history of code expansion. Here we re-examine the biochemical basis of this theory to test the validity of its statistical support. We show that the theory's definition of "precursor-product" amino acid pairs is unjustified biochemically because it requires the energetically unfavorable reversal of steps in extant metabolic pathways to achieve desired relationships. In addition, the theory neglects important biochemical constraints when calculating the probability that chance could assign precursor-product amino acids to contiguous codons. A conservative correction for these errors reveals a surprisingly high 23% probability that apparent patterns within the code are caused purely by chance. Finally, even this figure rests on post hoc assumptions about primordial codon assignments, without which the probability rises to 62% that chance alone could explain the precursor-product pairings found within the code. Thus we conclude that coevolution theory cannot adequately explain the structure of the genetic code.

Codon↗

Sexual reproduction as an adaptation to resist parasites (a review).

Darwinian theory has yet to explain adequately the fact of sex. If males provide little or no aid to offspring, a high (up to 2-fold) extra average fitness has to emerge as a property of a sexual parentage if sex is to be stable. The advantage must presumably come from recombination but has been hard to identify. It may well lie in the necessity to recombine defenses to defeat numerous parasites. A model demonstrating this works best for contesting hosts whose defense polymorphisms are constrained to low mutation rates. A review of the literature shows that the predictions of parasite coevolution fit well with the known ecology of sex. Moreover, parasite coevolution is superior to previous models of the evolution of sex by supporting the stability of sex under the following challenging conditions: very low fecundity, realistic patterns of genotype fitness and changing environment, and frequent mutation to parthenogenesis, even while sex pays the full 2-fold cost.

Adaptation, Biological↗

Menstruation: a nonadaptive consequence of uterine evolution.

Although adaptive explanations for menstruation go back at least twenty-five hundred years, in the last decade two new hypotheses have been advanced. The first suggests that menstruation evolved to cleanse the uterus of pathogens introduced by sperm, and the second argues that the function of endometrial regression (with the associated menstruation in humans) is to save energy by getting rid of tissue, rather than maintaining it in the absence of an available blastocyst. Both these suggestions may be questioned on the grounds that they do not take into account the physiology of the reproductive processes involved. Menstruation is not an independent physiological process and is unlikely to have been selected for independently of the evolutionary events that led to it. Furthermore, most primitive menstruating animals would have menstruated infrequently, and many may have reproduced or died without ever menstruating. In order to provide a context for understanding how menstruation may have come about, the evolution of the female vertebrate reproductive tract is briefly reviewed. In later stages, the coevolution of the embryo and uterus resulted in an intimate association between the trophoblast and the uterine blood vessels. As the embryo became more invasive, the uterus responded with increased cellular growth and differentiation of the endometrium to accommodate it. This reached its peak in mammals (such as rodents and humans), where the embryo passes through the epithelium into the endometrial stroma, which responds with differentiation of cells and blood vessels. Progesterone, secreted after ovulation, plays a crucial role in preparation for pregnancy. In addition to its well-known effects on the uterus, progesterone may be important in suppressing the inflammatory reaction that would be expected in response to the presence of a foreign body, such as an embryo. It is also suggested that vascular and cellular differentiation of the endometrial stroma has evolved by adaptation of the inflammatory (granulation tissue) reaction. When progesterone levels fall at the end of the cycle, there is tissue breakdown and bleeding. The uterus then reforms for the next ovulatory cycle. It is shown that the female reproductive tract has multiple functions that must occur in sequence. The coevolution of the embryo and maternal tract thus led to the close contact of two genetically different tissues, and problems such as the inflammatory reaction had to be overcome. Menstruation is a necessary consequence of these evolutionary changes, and needed no adaptive value in order to evolve.

Adaptation, Physiological↗

Patterns of genetic structure among populations of an oligophagous pollinating yucca moth (Tegeticula yuccasella).

Plant-insect associations have served as models for investigations of coevolution and the influence of biotic interactions on diversification. The pollination association between yuccas and yucca moths is a classic example of an obligate mutualism often suggested to have been affected by coevolution. Recent work has shown high host specificity in pollinating yucca moths, and here we use Tegeticula yuccasella, the species with the widest diet breadth, to ask how host specificity and isolation by distance contribute to specialization. Isolation by distance at a regional scale was observed in nucleotide variation within the mitochondrial gene cytochrome oxidase I (COI) (r =.294; P =.003). Host-related genetic structure (F(ct) = 0.08) was found to be slightly lower than the level of structure observed between eastern and western moth populations (F(ct) = 0.096). However, 56% of the COI haplotypes sampled from moths on Yucca filamentosa mapped to a host-specific clade in the haplotype network. Taken together, these results suggest that differentiation among T. yuccasella populations on alternative hosts is slight, but gene flow is influenced by both host association and geographic distance.

Animals↗

Evolutionary relationships among California serogroup viruses (Bunyaviridae) and Aedes mosquitoes (Diptera: Culicidae)

More than 100 published and four unpublished papers recording virus isolations of California (CAL) serogroup viruses from mosquitoes and other arthropods were analyzed, followed by a comparison of a contemporary classification of mosquitoes of the genus Aedes with a contemporary classification of CAL serogroup viruses. Using criteria of five or more total isolations of a given virus from a given species of mosquito, and a minimum infection rate of 1:10,000 or greater (more frequent), Aedes, and to a lesser extent Culiseta, species were found to be the arthropods most frequently involved as vectors. Such a comparison could not explain all virus-vector associations on the basis of coevolution of viruses in Aedes mosquito species, probably because of the crossing over of viruses to other mosquito species through horizontal transmission and because of deficiencies in currently available classifications. Coevolution of host-parasite systems is discussed, as are the inadequacies of contemporary taxonomic treatments of viruses and Aedes mosquitoes. The paper ends with hypothetical reconstructions of virus-mosquito relationships over time and possible routes of dispersal of California serogroup viruses to their present geographical distributions.

Aedes↗

The evolution of SMC proteins: phylogenetic analysis and structural implications.

The SMC proteins are found in nearly all living organisms examined, where they play crucial roles in mitotic chromosome dynamics, regulation of gene expression, and DNA repair. We have explored the phylogenetic relationships of SMC proteins from prokaryotes and eukaryotes, as well as their relationship to similar ABC ATPases, using maximum-likelihood analyses. We have also investigated the coevolution of different domains of eukaryotic SMC proteins and attempted to account for the evolutionary patterns we have observed in terms of available structural data. Based on our analyses, we propose that each of the six eukaryotic SMC subfamilies originated through a series of ancient gene duplication events, with the condensins evolving more rapidly than the cohesins. In addition, we show that the SMC5 and SMC6 subfamily members have evolved comparatively rapidly and suggest that these proteins may perform redundant functions in higher eukaryotes. Finally, we propose a possible structure for the SMC5/SMC6 heterodimer based on patterns of coevolution.

ATP-Binding Cassette Transporters↗

Networks of coevolving sites in structural and functional domains of serpin proteins.

Amino acids do not occur randomly in proteins; rather, their occurrence at any given site is strongly influenced by the amino acid composition at other sites, the structural and functional aspects of the region of the protein in which they occur, and the evolutionary history of the protein. The goal of our research study is to identify networks of coevolving sites within the serpin proteins (serine protease inhibitors) and classify them as being caused by structural-functional constraints or by evolutionary history. To address this, a matrix of pairwise normalized mutual information (NMI) values was computed among amino acid sites for the serpin proteins. The NMI matrix was partitioned into orthogonal patterns of amino acid variability by factor analysis. Each common factor pattern was interpreted as having phylogenetic and/or structural-functional explanations. In addition, we used a bootstrap factor analysis technique to limit the effects of phylogenetic history on our factor patterns. Our results show an extensive network of correlations among amino acid sites in key functional regions (reactive center loop, shutter, and breach). Additionally, we have discovered long-range coevolution for packed amino acids within the serpin protein core. Lastly, we have discovered a group of serpin sites which coevolve in the hydrophobic core region (s5B and s4B) and appear to represent sites important for formation of the "native" instead of the "latent" serpin structure. This research provides a better understanding on how protein structure evolves; in particular, it elucidates the selective forces creating coevolution among protein sites.

Amino Acids↗

Functional promiscuity of squirrel monkey growth hormone receptor toward both primate and nonprimate growth hormones.

Primate growth hormone (GH) has evolved rapidly, having undergone approximately 30% amino acid substitutions from the inferred ancestral eutherian sequence. Nevertheless, human growth hormone (hGH) is physiologically effective when administered to nonprimate mammals. In contrast, its functional counterpart, the human growth hormone receptor (hGHR), has evolved species specificity so that it responds only to Old World primate GHs. It has been proposed that this species specificity of the hGHR is largely caused by the Leu --> Arg change at position 43 after a prior His --> Asp change at position 171 of the GH. Sequence analyses supported this hypothesis and revealed that the transitional phase in the GH:GHR coevolution still persists in New World monkeys. For example, although the GH of the squirrel monkey has the His --> Asp substitution at position 171, residue 43 of its GHR is a Leu, the nonprimate residue. If the squirrel monkey truly represents an intermediate stage of GH:GHR coevolution, its GHR should respond to both hGH and nonprimate GH. Also, if the emergence of species specificity was a result of the selection for a more efficient GH:GHR interaction, then changing residue 43 of the squirrel monkey growth hormone receptor (smGHR) to Arg should increase its binding affinity toward higher primate GH. To test these hypotheses, we performed protein-binding assays between the smGHR and both human and rat GHs, using the surface plasmon resonance methodology. Furthermore, the effects of reciprocal mutations at position 43 of human and squirrel monkey GHRs are measured for their binding affinities toward human and squirrel monkey GHs. The results from the binding kinetic assays clearly demonstrate that the smGHR is in the intermediate state of the evolution of species specificity. Interestingly, the altered residue Arg at position 43 of the smGHR does not lead to an increased binding affinity. The implications of these results on the evolution of the GH:GHR interaction and on functional evolution are discussed.

Animals↗

Geographical variation and sexual dimorphism of phenoloxidase levels in Japanese beetles (Popillia japonica).

Phenoloxidase (PO) production can be used as an indicator of pathogen defence in insects. The geographical mosaic of coevolution implies that traits associated with pathogen defence will vary across a geographical range. Bateman's principle implies that the benefit of increased defence levels is greater for females than males. To test both of these hypotheses, we sampled four populations of Japanese beetles, Popillia japonica, across Vermont: two were from locations using biological pest control, and two locations did not use biocontrol. We quantified defence levels (PO) and parasite resistance in males and females from each population. Populations from areas with biocontrol exhibited greater PO production, females produced more PO, populations with higher levels of PO suffered less mortality from pathogen exposure, and PO levels positively correlate with increased mortality in the absence of parasitism. Results support the geographical mosaic of coevolution and the implications of Bateman's principle.

Analysis of Variance↗

Intraspecific phylogenetic congruence among multiple symbiont genomes.

Eukaryotes often form intimate endosymbioses with prokaryotic organisms. Cases in which these symbionts are transmitted cytoplasmically to host progeny create the potential for co-speciation or congruent evolution among the distinct genomes of these partners. If symbionts do not move horizontally between different eukaryotic hosts, strict phylogenetic congruence of their genomes is predicted and should extend to relationships within a single host species. Conversely, even rare 'host shifts' among closely related lineages should yield conflicting tree topologies at the intraspecific level. Here, we investigate the historical associations among four symbiotic genomes residing within an aphid host: the mitochondrial DNA of Uroleucon ambrosiae aphids, the bacterial chromosome of their Buchnera bacterial endosymbionts, and two plasmids associated with Buchnera. DNA sequence polymorphisms provided a significant phylogenetic signal and no homoplasy for each data set, yielding completely and significantly congruent phylogenies for these four genomes and no evidence of horizontal transmission. This study thus provides the first evidence for strictly vertical transmission and 'co-speciation' of symbiotic organisms at the intraspecific level, and represents the lowest phylogenetic level at which such coevolution has been demonstrated. These results may reflect the obligate nature of this intimate mutualism and indicate opportunities for adaptive coevolution among linked symbiont genomes.

Animals↗

Sexual conflict and cooperation in butterfly reproduction: a comparative study of polyandry and female fitness.

Most butterfly species can be characterized as capital breeders, meaning that reproductive output is strongly coupled to the amount of resources they have procured during the larval stage. Accordingly, female fecundity is generally correlated with female mass, both within and across species. However, the females of some species can be partly characterized as income breeders, in the sense that their reproductive output is dependent not only on larval-derived capital but also on resources acquired during the adult stage. These adult resources can be derived from female feeding or from male-transferred nuptial gifts. Recent studies on the within-species effects of multiple matings on female fitness show that females generally gain directly from multiple matings in terms of increased lifetime offspring production. Here, we test whether the positive effects of multiple mating on female fitness also hold at a comparative level, by conducting a laboratory study of female reproductive output in eight pierid species that differ in life-time female mating frequency. Female reproductive output, measured as cumulative egg mass divided by female mass, increased significantly with polyandry (r = 0.942, p < 0.001), demonstrating that the positive effect of mating rate on female reproductive fitness also holds between species. The positive effect of male nutrient contribution is substantial, and the per capita reproductive output is more than twice as high in the most polyandrous species as in the most monandrous ones. Hence, the positive net effect of the ejaculates is highly substantial, although males and females can have sexual interests that run counter to each other, setting the stage for sexually antagonistic coevolution, so that the various component parts of the male ejaculate-sperm, nutrients, anti-aphrodisiacs, and gonadotrophic hormones-may each correspond to a separate conflict-cooperation balance between the sexes. Two scenarios for the evolution of nuptial gifts in butterflies are discussed, one arguing that variation in larval food is the underlying factor and the other arguing that sexually antagonistic coevolution is the driving force. The two views are complementary rather than mutually exclusive, although the former hypothesis predicts that variation in female mating rate depends on variation in larval food availability, whereas the latter suggests that variation in female mating rate between species results from species-specific idiosyncrasies.

Animals↗

Conservation and divergence in multigene families: alternatives to selection and drift.

It is generally assumed that conservation and divergence of DNA signify function (selection) and no function (drift), respectively. This assumption is based on the view that a mutation is a unique event on a single chromosome, the fate of which depends on selection or drift. Knowledge of the rates, units and biases of widespread mechanisms of non-reciprocal DNA exchange, in particular within multigene families, provides alternative explanations for conservation and divergence, notwithstanding biological function. Such mechanisms of DNA turnover cause continual fluctuations in the copy-number of variant genes in an individual and, hence, promote the gradual and cohesive spread of a variant gene throughout a family (homogenization) and throughout a population (fixation). The dual processes (molecular drive) of homogenization and fixation are inextricably linked. Data are presented of the expected stages of transition in the spread of variant repeats by molecular drive in some non-genic families of DNA, seemingly not under the influence of selection. When a molecularly driven change in a given gene family is accompanied by the coevolution (mediated by selection) of other DNA, RNA or protein molecules that interact with the gene family then biological function is observed to be maintained despite sequence divergence. Conversely, the mechanics of DNA turnover and a turnover bias in favour of ancestral sequences can dramatically retard the rate of sequence change, in the absence of function. Examples of the maintenance of function by molecular coevolution and conservation of sequences in the absence of function, are drawn mainly from the rDNA multigene family.

Animals↗

Assessing sexual conflict in the Drosophila melanogaster laboratory model system.

We describe a graphical model of interlocus coevolution used to distinguish between the interlocus sexual conflict that leads to sexually antagonistic coevolution, and the intrinsic conflict over mating rate that is an integral part of traditional models of sexual selection. We next distinguish the 'laboratory island' approach from the study of both inbred lines and laboratory populations that are newly derived from nature, discuss why we consider it to be one of the most fitting forms of laboratory analysis to study interlocus sexual conflict, and then describe four experiments using this approach with Drosophila melanogaster. The first experiment evaluates the efficacy of the laboratory model system to study interlocus sexual conflict by comparing remating rates of females when they are, or are not, provided with a spatial refuge from persistent male courtship. The second experiment tests for a lag-load in males that is due to adaptations that have accumulated in females, which diminish male-induced harm while simultaneously interfering with a male's ability to compete in the context of sexual selection. The third and fourth experiments test for a lag-load in females owing to direct costs from their interactions with males, and for the capacity for indirect benefits to compensate for these direct costs.

Animals↗