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Rapid coevolution of the nematode sex-determining genes fem-3 and tra-2.

Unlike many features of metazoan development, sex determination is not widely conserved among phyla. However, the recent demonstration that one gene family controls sexual development in Drosophila, C. elegans, and vertebrates suggests that sex determination mechanisms may have evolved from a common pathway that has diverged radically since the Cambrian. Sex determination gene sequences often evolve quickly, but it is not known how this relates to higher-order pathways or what selective or neutral forces are driving it. In such a rapidly evolving developmental pathway, the fate of functionally linked genes is of particular interest. To investigate a pair of such genes, we cloned orthologs of the key C. elegans male-promoting gene fem-3 from two sister species, C. briggsae and C. remanei. We employed RNA interference to show that in all three species, the male-promoting function of fem-3 and its epistatic relationship with its female-promoting upstream repressor, tra-2, are conserved. Consistent with this, the FEM-3 protein interacts with TRA-2 in each species, but in a strictly species-specific manner. Because FEM-3 is the most divergent protein yet described in Caenorhabditis and the FEM-3 binding domain of TRA-2 is itself hypervariable, a key protein-protein interaction is rapidly evolving in concert. Extrapolation of this result to larger phylogenetic scales helps explain the dissimilarity of the sex determination systems across phyla.

Amino Acid Sequence↗

The evolution of condition-dependent sexual dimorphism.

Theory suggests that the net benefit of allocating resources to a sexual trait depends both on the strength of sexual selection on that trait and on individual condition. This predicts a tight coevolution between sexual dimorphism and condition dependence and suggests that these patterns of within-sex and between-sex variation may share a common genetic and developmental basis. Although condition-dependent expression of sexual traits is widely documented, the extent of covariation between condition dependence and sexual dimorphism remains poorly known. I investigated the effects of condition (larval diet quality) on multivariate sexual dimorphism in the fly Telostylinus angusticollis (Neriidae). Condition determined the direction of sexual size dimorphism and modulated sexual shape dimorphism by affecting allometric slopes and/or intercepts of sexually homologous traits in both sexes. Although the greatest responses to condition manipulation were observed in male sexual traits, both sexual and nonsexual traits exhibited substantial variation in the nature and magnitude of condition effects. Nonetheless, condition dependence and sexual dimorphism were remarkably congruent: variation in the strength of condition effects on male traits explained more than 90% of the variation in the magnitude of sexual dimorphism, whether quantified in terms of trait size or allometric slope. The genetic mechanisms that give rise to multivariate sexual dimorphism in body shape thus function in a strongly condition-dependent manner in this species, suggesting a common genetic basis for body shape variation within and between sexes.

Animals↗

Coevolution of hosts and microorganisms: an analysis of the involvement of cytokines in host-parasite interactions.

Parasites may employ particular strategies of eluding an immune response by taking advantage of those mechanisms that normally guarantee immunological self-tolerance. Much in the way as it occurs during the establishment of self-tolerance, live pathogens may induce clonal deletion, functional inactivation (anergy) and immunosuppression. At this latter level, it appears that certain pathogens produce immunosuppressive cytokine-like mediators or provoke the host to secrete cytokines that will compromise the anti-parasite immune response. It appears that immune responses that preferentially involve T helper 1 cells (secretors of interleukin-2-and interferon-gamma) tend to be protective, whereas T helper 2 cells (secretors of IL-4, IL-5, IL-6, and IL-10), a population that antagonizes T helper cells, mediate disease susceptibility and are involved in immunopathological reactions. Cytokines produced by T helper 2 cells mediate many symptoms of infection, including eosinophilia, mastocytosis, hyperimmunoglobulinemia, and elevated IgE levels. Administration of IL-2 and IFN-gamma has beneficial effects in many infections mediated by viruses, bacteria, and protozoa. The use of live vaccinia virus might be an avenue for the treatment of or the vaccination against infection. We have found that a vaccinia virus expressing the gene for human IL-2, though attenuated, precipitates autoimmune disease in immunodeficient, athymic mice. Thus, although T helper 1 cytokines may have desired immunostimulatory properties, they also may lead to unwarranted autoaggressive responses.

Animals↗

Coevolution of an avian host and its parasitic cuckoo.

We use a quantitative genetic model to examine the coevolution of host and cuckoo egg characters (termed "size" as a proxy for general appearance), host discrimination, and host and cuckoo population dynamics. A host decides whether to discard an egg using a comparison of the sizes of the eggs in her nest, which changes as host and cuckoo eggs evolve. Specifically, we assume that the probability that she discards the largest egg in her nest depends on how much larger it is than the second largest egg. This decision rule (i.e., the acceptable difference in egg sizes) also evolves, changing both the chance of successful rejection of a cuckoo egg in parasitized nests and the chance of mistaken rejection of a host egg in both parasitized and unparasitized nests. We find a stable equilibrium for coexistence of the host and cuckoo where there is cuckoo egg mimicry, evolutionary displacement of the host egg away from the cuckoo egg phenotype, and host discrimination against unusual eggs. Both host discrimination and host egg displacement are fairly weak at the equilibrium. Cuckoo egg mimicry, although imperfect, usually evolves more extensively and quickly than the responses of the host. Our model provides evidence for both the evolutionary equilibrium and evolutionary lag hypotheses of host acceptance of parasitic eggs.

Animals↗

Coevolutionary networks: a novel approach to understanding the relationships of humans with the infectious agents.

Human organism is interpenetrated by the world of microorganisms, from the conception until the death. This interpenetration involves different levels of interactions between the partners including trophic exchanges, bi-directional cell signaling and gene activation, besides genetic and epigenetic phenomena, and tends towards mutual adaptation and coevolution. Since these processes are critical for the survival of individuals and species, they rely on the existence of a complex organization of adaptive systems aiming at two apparently conflicting purposes: the maintenance of the internal coherence of each partner, and a mutually advantageous coexistence and progressive adaptation between them. Humans possess three adaptive systems: the nervous, the endocrine and the immune system, each internally organized into subsystems functionally connected by intraconnections, to maintain the internal coherence of the system. The three adaptive systems aim at the maintenance of the internal coherence of the organism and are functionally linked by interconnections, in such way that what happens to one is immediately sensed by the others. The different communities of infectious agents that live within the organism are also organized into functional networks. The members of each community are linked by intraconnections, represented by the mutual trophic, metabolic and other influences, while the different infectious communities affect each other through interconnections. Furthermore, by means of its adaptive systems, the organism influences and is influenced by the microbial communities through the existence of transconnections. It is proposed that these highly complex and dynamic networks, involving gene exchange and epigenetic phenomena, represent major coevolutionary forces for humans and microorganisms.

Adaptation, Physiological↗

Ecological and reproductive character displacement on an environmental gradient.

Character displacement, in which coevolution of similar species alters their phenotypes, can be difficult to identify on the basis of observational data alone. In two-species systems, the most commonly identified (i.e., classic) resulting pattern is greater phenotypic difference between species in sympatry than allopatry. We show that restricting studies to this pattern may exclude many instances of character displacement, particularly in the presence of spatial environmental gradients. We present four spatial models of character displacement in quantitative traits affecting competition and hybridization between the species. Our models highlight the connections between range limits and character displacement in continuous space. We conclude that the classic pattern is less likely to occur for a trait affecting resource acquisition than for a trait affecting mate choice. We also show that interspecific hybridization (when hybrids are inviable), even in very small amounts, has marked effects on the shape and stability of borders between species and the nature of character displacement. A survey of the empirical literature shows that character displacement studies often lack analysis of spatial phenotype and abundance data. We recommend more careful spatial sampling in character displacement studies, and we illustrate how comparison of clines in mean phenotype in sympatry and allopatry can be used to suggest the action of character displacement.

Animals↗

Seabird and louse coevolution: complex histories revealed by 12S rRNA sequences and reconciliation analyses.

We investigated the coevolutionary history of seabirds (orders Procellariiformes and Sphenisciformes) and their lice (order Phthiraptera). Independent trees were produced for the seabirds (tree derived from 12S ribosomal RNA, isoenzyme, and behavioral data) and their lice (trees derived from 12S rRNA data). Brook's parsimony analysis (BPA) supported a general history of cospeciation (consistency index = 0.84, retention index = 0.81). We inferred that the homoplasy in the BPA was caused by one intrahost speciation, one potential host-switching, and eight or nine sorting events. Using reconciliation analysis, we quantified the cost of fitting the louse tree onto the seabird tree. The reconciled trees postulated one host-switching, nine cospeciation, three or four intrahost speciation, and 11 to 14 sorting events. The number of cospeciation events was significantly more than would be expected from chance alone (P < 0.01). The sequence data were used to test for rate heterogeneity for both seabirds and lice. Neither data set displayed significant rate heterogeneity. An examination of the codivergent nodes revealed that seabirds and lice have cospeciated synchronously and that lice have evolved at approximately 5.5 times the rate of seabirds. The degree of sequence divergence supported some of the postulated intrahost speciation events (e.g., Halipeurus predated the evolution of their present hosts). The sequence data also supported some of the postulated host-switching events. These results demonstrate the value of sequence data and reconciliation analyses in unraveling complex histories between hosts and their parasites.

Animals↗

A model for the coevolution of the genetic code and the process of protein synthesis: Review and assessment.

The contemporary genetic code and the process of protein biosynthesis most assuredly evolved from a simpler code and process. We believe that there was obligatory coevolution of the two and that the earlier code and process must have involved a more direct linkage between the amino acids and the information macromolecule. We propose that an early form of translating existed in which amino acids were attached directly to the 'messenger' RNA along the backbone as 2'OH aminoacyl esters. These esters then condensed with each other on the RNA backbone yielding a peptide covalently attached to the RNA, without the use of tRNA's and ribosomes. THis presentation is concerned with experimental data which indicate that such a simple translation system is possible and must have involved the following steps: (1) formation of the aminoacyl adenylate anhydride, (2) transfer of the amino acid from the adenylate to immidazole, (3) transfer of the amino acid from imidazole to 2'OH groups along the backbone of RNAs, (4) condensation of the amino acids to yield peptides. Steps (1)-(3) have been confirmed in chemical systems. Our preliminary evidence indicates step (4) is also possible. The aminoacylation of polyribonucleotides and the subsequent formation of peptides is a dynamic and experimentally accessible system for studying genetic coding specfities and our present studies are now concentrated on step (4), looking for such specifities.

Acylation↗

Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counterdefense mechanism by plant pathogens.

A characteristic plant response to microbial attack is the production of endo-beta-1,3-glucanases, which are thought to play an important role in plant defense, either directly, through the degradation of beta-1,3/1,6-glucans in the pathogen cell wall, or indirectly, by releasing oligosaccharide elicitors that induce additional plant defenses. We report the sequencing and characterization of a class of proteins, termed glucanase inhibitor proteins (GIPs), that are secreted by the oomycete Phytophthora sojae, a pathogen of soybean, and that specifically inhibit the endoglucanase activity of their plant host. GIPs are homologous with the trypsin class of Ser proteases but are proteolytically nonfunctional because one or more residues of the essential catalytic triad is absent. However, specific structural features are conserved that are characteristic of protein-protein interactions, suggesting a mechanism of action that has not been described previously in plant pathogen studies. We also report the identification of two soybean endoglucanases: EGaseA, which acts as a high-affinity ligand for GIP1; and EGaseB, with which GIP1 does not show any association. In vitro, GIP1 inhibits the EGaseA-mediated release of elicitor-active glucan oligosaccharides from P. sojae cell walls. Furthermore, GIPs and soybean endoglucanases interact in vivo during pathogenesis in soybean roots. GIPs represent a novel counterdefensive weapon used by plant pathogens to suppress a plant defense response and potentially function as important pathogenicity determinants.

Amino Acid Sequence↗

Evolutionary cycling in predator-prey interactions: population dynamics and the red queen.

This paper describes the coevolution of phenotypes in a community comprising a population of predators and of prey. It is shown that evolutionary cycling is a likely outcome of the process. The dynamical systems on which this description is based are constructed from microscopic stochastic birth and death events, together with a process of random mutation. Births and deaths are caused in part by phenotype-dependent interactions between predator and prey individuals and therefore generate natural selection. Three outcomes of evolution are demonstrated. A community may evolve to a state at which the predator becomes extinct, or to one at which the species coexist with constant phenotypic values, or the species may coexist with cyclic changes in phenotypic values. The last outcome corresponds to a Red Queen dynamic, in which the selection pressures arising from the predator-prey interaction cause the species to evolve without ever reaching an equilibrium phenotypic state. The Red Queen dynamic requires an intermediate harvesting efficiency of the prey by the predator and sufficiently high evolutionary rate constant of the prey, and is robust when the model is made stochastic and phenotypically polymorphic. A cyclic outcome lies outside the contemporary focus on evolutionary equilibria, and argues for an extension to a dynamical framework for describing the asymptotic states of evolution.

Animals↗

Extensive exchange of fungal cultivars between sympatric species of fungus-growing ants.

Fungal cultivars of fungus-growing ants (Attini, Formicidae) are carried by dispersing queens from parent to offspring nest. This vertical cultivar transmission between generations is thought to result in long-term ant-fungus coevolution and selection for beneficial cultivar traits that maximize harvests and thus colony productivity. In contrast to this traditional view of vertical cultivar transmission, frequent horizontal cultivar transmission between ant species is implicated by a phylogenetic analysis of 72 cultivars propagated by two fungus-growing ant species coexisting sympatrically in central Panama. The two ant species are specialized on the same group of closely related cultivars, but in six of 12 cultivar clades identifiable within this group, cultivars from both ant species were united in the same clade. Five of these 'mixed' clades were supported by bootstrap values of about 90% or higher. In one instance, colonies from the two ant species cultivated the same, genetically identical, cultivar clone. These phylogenetic patterns indicate that: (i) cultivar exchanges between the two ant species occur routinely throughout ecological time; and that (ii) coevolutionary processes between ants and their fungi are more diffuse than previously assumed. Because the two ant species are specialized on a narrow group of closely related cultivars that they regularly exchange among each other, but not with other sympatric ant species, cultivar exchanges are constrained, most likely, by ant preferences for their own cultivar group or by stringent selection against transitions of ant lineages to distantly related cultivars.

Animals↗

Toward a theory for the evolution of cultural communication: coevolution of signal transmission and reception.

A haploid sexual two-locus model of gene-culture coevolution is examined, in which a dichotomous phenotype subject to natural selection is transmitted vertically with probabilities dependent on the chosen parent's genotype and phenotype and the offspring's genotype. Stability conditions for the genetically monomorphic corner equilibria are obtained. In a specialization of this general model, one locus controls the transmission and the other controls the reception of adaptive information. The corner and edge equilibria of this doubly coevolutionary model are fully analyzed, and conditions for transmission and reception to coevolve are derived in terms of the efficiency of vertical transmission, the selective advantage gained from possessing the information, the costs of transmission and reception, and the recombination fraction between the two loci. Possible applications of the model are to the evolution of semantic alarm calls in vervet monkeys and the phonetic aspects of human language. In a third model with diploid genetics, we consider the initial increase of cultural transmission from a mutation-selection balance in which the adaptive phenotype is the consequence of a dominant gene at one locus. A second gene controls the transmission of the phenotype in such a way that a new mutant at this second locus permits learning of the adaptive phenotype from a parent who has it. This new mutant cannot increase when rare.

Animal Communication↗

A model for tool-use traditions in primates: implications for the coevolution of culture and cognition.

Inspired by the demonstration that tool-use variants among wild chimpanzees and orangutans qualify as traditions (or cultures), we developed a formal model to predict the incidence of these acquired specializations among wild primates and to examine the evolution of their underlying abilities. We assumed that the acquisition of the skill by an individual in a social unit is crucially controlled by three main factors, namely probability of innovation, probability of socially biased learning, and the prevailing social conditions (sociability, or number of potential experts at close proximity). The model reconfirms the restriction of customary tool use in wild primates to the most intelligent radiation, great apes; the greater incidence of tool use in more sociable populations of orangutans and chimpanzees; and tendencies toward tool manufacture among the most sociable monkeys. However, it also indicates that sociable gregariousness is far more likely to produce the maintenance of invented skills in a population than solitary life, where the mother is the only accessible expert. We therefore used the model to explore the evolution of the three key parameters. The most likely evolutionary scenario is that where complex skills contribute to fitness, sociability and/or the capacity for socially biased learning increase, whereas innovative abilities (i.e., intelligence) follow indirectly. We suggest that the evolution of high intelligence will often be a byproduct of selection on abilities for socially biased learning that are needed to acquire important skills, and hence that high intelligence should be most common in sociable rather than solitary organisms. Evidence for increased sociability during hominin evolution is consistent with this new hypothesis.

Animals↗

Costly traumatic insemination and a female counter-adaptation in bed bugs.

Male bed bugs pierce females through the body wall and inseminate directly into the body cavity. It has previously been shown that such traumatic insemination carries costs for females, and sexual conflict regarding the mode of insemination should thus propel male-female coevolution. Since males accumulate sexually antagonistic adaptations, females should evolve counter-adaptations that efficiently abate the costs to females of sexual interactions. Yet, unambiguous experimental evidence for female counter-adaptations is lacking. In bed bugs, the spermalege (a highly modified region of the abdomen where the male usually pierces the female) may represent a female counter-adaptation. We assess the female costs of traumatic insemination by varying the rate of insemination on the one hand, and the rate and mode of piercing trauma to females on the other. Our results show that female mating costs are not extreme-elevated mating rate shortened female lifespan but had no significant effect on lifetime egg production. More importantly, additional abdominal piercing in the spermalege had no effect on females whereas even a very low rate of such piercing outside the spermalege reduced female lifetime egg production by 50%. Thus, females are well counter-adapted to the intrusive mode of insemination exhibited by male bed bugs and the costs of elevated mating are comparable with those in other insects, as predicted by theory. We therefore demonstrate that the spermalege efficiently reduces the direct costs of piercing trauma to females, and hence provide experimental evidence for a female counter-adaptation to a sexually antagonistic male trait.

Adaptation, Biological↗

Coevolution of recovery ability and virulence.

Most models for coevolution of hosts and parasites are based on the assumption that resistance of hosts to parasites is an all-or-nothing effect. In many cases, for example where parasites require an appropriate receptor on host cells, this is a reasonable assumption. However, in many other cases, for example where hosts mount an immune response, this picture may be too simple. An immune system is expensive to maintain, which poses a question as to how much of its resources a host should allocate to resist parasites: if the risk of infection is low, natural selection may favour hosts with less effective immune systems. As optimal allocation to defence will depend on the force of infection, and the force of infection, in turn, depends on the level of defence in the rest of the host population, a game-theoretic approach is necessary. Here I analyse a simple model for the evolution of the ability to recover from infection. If parasites are not allowed to coevolve, the outcome is a single evolutionarily stable strategy (ESS). If the parasites coevolve, multiple evolutionary outcomes are possible, one in which the parasites are relatively avirulent and common and the hosts invest little in recovery ability, and another (the escalated arms race) where parasites are rare but virulent and the hosts invest heavily in defence.

Animals↗

Warning displays in spiny animals: one (more) evolutionary route to aposematism.

To date, theoretical or laboratory simulations of aposematic evolution in prey animals have focused narrowly on internally stored chemical defense as the source of unprofitability and ignore aposematic advertisement of physical defenses such as spines (and defensive hairs, claws, etc.). This has occurred even though aposematism in spiny animals has been recognized since the 19th century. In this paper we present the first detailed theoretical consideration of aposematism in spiny animals, focusing on questions of initial evolution, costs of display, and coevolution of displays with defenses. Using an individual-based evolutionary model, we found that spines (or similar physical defenses) can easily evolve without aposematism, but when spines do evolve, aposematic displays can also easily evolve if they help to make the prey animal distinctive and if they draw attention to the physical threat. When aposematic displays evolve, they cause reduced investment in costly spines, so that, in addition to signaling unprofitability, aposematic display may enhance the cost-effectiveness of antipredator defenses (one exception to this conclusion is if the display is itself as costly as the defense). For animals with stinging spines, combining physical and chemical defense, the evolution of aposematic display may lead to reduced investment in the toxin compared to the spine. This occurs because spines act as both secondary (repellent) defenses and as primary defenses (their own visible, honest advertisement), whereas internally stored toxins only (generally) act as repellent secondary defenses. We argue that conspicuous aposematism in spines functions as an attention-getting mechanism, whereas conspicuous aposematic display in purely toxic animals may be explained by signal reliability arguments. Finally, one (more) route by which aposematism may initially evolve is by spiny rather than purely chemically defended species, spreading to species with other forms of secondary defense as the signal becomes common.

Animal Structures↗

Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host.

We investigated the bacterial gut microbiota from 32 colonies of wood-feeding termites, comprising four Microcerotermes species (Termitidae) and four Reticulitermes species (Rhinotermitidae), using terminal restriction fragment length polymorphism analysis and clonal analysis of 16S rRNA. The obtained molecular community profiles were compared statistically between individuals, colonies, locations, and species of termites. Both analyses revealed that the bacterial community structure was remarkably similar within each termite genus, with small but significant differences between sampling sites and/or termite species. In contrast, considerable differences were found between the two termite genera. Only one bacterial phylotype (defined with 97% sequence identity) was shared between the two termite genera, while 18% and 50% of the phylotypes were shared between two congeneric species in the genera Microcerotermes and Reticulitermes, respectively. Nevertheless, a phylogenetic analysis of 228 phylotypes from Microcerotermes spp. and 367 phylotypes from Reticulitermes spp. with other termite gut clones available in public databases demonstrated the monophyly of many phylotypes from distantly related termites. The monophyletic "termite clusters" comprised of phylotypes from more than one termite species were distributed among 15 bacterial phyla, including the novel candidate phyla TG2 and TG3. These termite clusters accounted for 95% of the 960 clones analyzed in this study. Moreover, the clusters in 12 phyla comprised phylotypes from more than one termite (sub)family, accounting for 75% of the analyzed clones. Our results suggest that the majority of gut bacteria are not allochthonous but are specific symbionts that have coevolved with termites and that their community structure is basically consistent within a genus of termites.

Animals↗

Coevolution of host and virus: the pathogenesis of virulent and attenuated strains of myxoma virus in resistant and susceptible European rabbits.

Myxoma virus was introduced into the European rabbit population of Australia in 1950. Although the virus was initially highly lethal in rabbits, there was rapid selection for less virulent strains of virus and innately resistant rabbits. To investigate the basis of resistance to myxoma virus, we have compared the pathogensis of the virulent strain of myxoma virus originally released into Australia and an attenuated, naturally derived field strain of myxoma virus. This was done in laboratory rabbits, which have not been selected for resistance, and in wild rabbits that have developed significant resistance. Wild rabbits were able to recover from infection with virus that was always lethal in laboratory rabbits. Laboratory rabbits were able to control and recover from infection with attenuated virus. This virus caused a trivial disease in wild rabbits. There was little difference between laboratory and wild rabbits in titers of either virulent or attenuated virus in the skin at the inoculation site. However, resistant wild rabbits had a 10- to 100-fold lower titer of virulent virus within the lymph node draining the inoculation site and controlled virus replication in tissues distal to the draining lymph node. Replication of virus in lymphocytes or fibroblasts cultured from wild and laboratory rabbits demonstrated that resistance was not due to altered cellular permissivity for replication. Neutralizing antibodies were present in both susceptible and resistant rabbits, suggesting that these have no significant role in resistance. We hypothesise that resistance is due to an enhanced innate immune response that allows the rabbit to mount an effective cellular immune response.

Animals↗