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Rapid divergence of the ecdysone receptor in Diptera and Lepidoptera suggests coevolution between ECR and USP-RXR.

Ecdysteroid hormones are major regulators in reproduction and development of insects, including larval molts and metamorphosis. The functional ecdysone receptor is a heterodimer of ECR (NR1H1) and USP-RXR (NR2B4), which is the orthologue of vertebrate retinoid X receptors (RXR alpha, beta, gamma). Both proteins belong to the superfamily of nuclear hormone receptors, ligand-dependent transcription factors that share two conserved domains: the DNA-binding domain (DBD) and the ligand-binding domain (LBD). In order to gain further insight into the evolution of metamorphosis and gene regulation by ecdysone in arthropods, we performed a phylogenetic analysis of both partners of the heterodimer ECR/USP-RXR. Overall, 38 USP-RXR and 19 ECR protein sequences, from 33 species, have been used for this analysis. Interestingly, sequence alignments and structural comparisons reveal high divergence rates, for both ECR and USP-RXR, specifically among Diptera and Lepidoptera. The most impressive differences affect the ligand-binding domain of USP-RXR. In addition, ECR sequences show variability in other domains, namely the DNA-binding and the carboxy-terminal F domains. Our data provide the first evidence that ECR and USP-RXR may have coevolved during holometabolous insect diversification, leading to a functional divergence of the ecdysone receptor. These results have general implications on fundamental aspects of insect development, evolution of nuclear receptors, and the design of specific insecticides.

Amino Acid Sequence↗

Conservation and coevolution in the scale-free human gene coexpression network.

The role of natural selection in biology is well appreciated. Recently, however, a critical role for physical principles of network self-organization in biological systems has been revealed. Here, we employ a systems level view of genome-scale sequence and expression data to examine the interplay between these two sources of order, natural selection and physical self-organization, in the evolution of human gene regulation. The topology of a human gene coexpression network, derived from tissue-specific expression profiles, shows scale-free properties that imply evolutionary self-organization via preferential node attachment. Genes with numerous coexpressed partners (the hubs of the coexpression network) evolve more slowly on average than genes with fewer coexpressed partners, and genes that are coexpressed show similar rates of evolution. Thus, the strength of selective constraints on gene sequences is affected by the topology of the gene coexpression network. This connection is strong for the coding regions and 3' untranslated regions (UTRs), but the 5' UTRs appear to evolve under a different regime. Surprisingly, we found no connection between the rate of gene sequence divergence and the extent of gene expression profile divergence between human and mouse. This suggests that distinct modes of natural selection might govern sequence versus expression divergence, and we propose a model, based on rapid, adaptation-driven divergence and convergent evolution of gene expression patterns, for how natural selection could influence gene expression divergence.

3' Untranslated Regions↗

The coevolution of insect muscle TpnT and TpnI gene isoforms.

In bilaterians, the main regulator of muscle contraction is the troponin (Tpn) complex, comprising three closely interacting subunits (C, T, and I). To understand how evolutionary forces drive molecular change in protein complexes, we have compared the gene structures and expression patterns of Tpn genes in insects. In this class, while TpnC is encoded by multiple genes, TpnT and TpnI are encoded by single genes. Their isoform expression pattern is highly conserved within the Drosophilidae, and single orthologous genes were identified in the sequenced genomes of Drosophila pseudoobscura, Anopheles gambiae, and Apis mellifera. Apis expression patterns also support the equivalence of their exon organization throughout holometabolous insects. All TpnT genes include a previously unidentified indirect flight muscle (IFM)-specific exon (10A) that has evolved an expression pattern similar to that of exon 9 in TpnI. Thus, expression patterns, sequence evolution trends, and structural data indicate that Tpn genes and their isoforms have coevolved, building species- and muscle-specific troponin complexes. Furthermore, a clear case can be made for independent evolution of the IFM-specific isoforms containing alanine/proline-rich sequences. Dipteran genomes contain one tropomyosin gene that encodes one or two high-molecular weight isoforms (TmH) incorporating APPAEGA-rich sequences, specifically expressed in IFM. Corresponding exons do not exist in the Apis tropomyosin gene, but equivalent sequences occur in a high-molecular weight Apis IFM-specific TpnI isoform (TnH). Overall, our approach to comparatively analyze supramolecular complexes reveals coevolutionary trends not only in gene families but in isoforms generated by alternative splicing.

Amino Acid Sequence↗

Coevolution of immunoglobulin heavy- and light-chain variable-region gene families.

The gene families encoding the immunoglobulin variable regions of heavy (VH) and light (VL) chains in vertebrates are composed of many genes. However, the gene number and the extent of diversity among VH and VL gene copies vary with species. To examine the causes of this variation and the evolutionary forces for these multigene families, we conducted a phylogenetic analysis of VH and VL genes from the species of amniotes. The results of our analysis showed that for each species, VH and VL genes have the same pattern of clustering in the trees, and, according to this clustering pattern, the species can be divided into two groups. In the first group of species (humans and mice), VH and VL genes were extensively intermingled with genes from other organisms; in the second group of species (chickens, rabbits, cattle, sheep, swine, and horses), the genes tended to form clusters within the same group of organisms. These results suggest that the VH and VL multigene families have evolved in the same fashion: they have undergone coordinated contraction and expansion of gene repertoires such that each group of organisms is characterized by a certain level of diversity of VH and VL genes. The extent of diversity among copies of VH and VL genes in each species is related to the mechanism of generation of antibody variety. In humans and mice, DNA rearrangement of immunoglobulin variable, diversity, and joining-segment genes is a main source of antibody diversity, whereas in chickens, rabbits, cattle, sheep, swine, and horses, somatic hypermutation and somatic gene conversion play important roles. The evolutionary pattern of VH and VL multigene families is consistent with the birth-and-death model of evolution, yet different levels of diversifying selection seem to operate in the VH and VL genes of these two groups of species.

Animals↗

Coevolution of the glucose dehydrogenase gene and the ejaculatory duct in the genus Drosophila.

The glucose dehydrogenase gene (Gld) in Drosophila melanogaster exhibits a unique spatial and temporal pattern of expression. GLD expression switches from a non-sex-limited state at the pupal stage to a male-limited state at the adult stage. At the adult stage, the enzyme is restricted to the ejaculatory duct. Within the genus Drosophila, the ejaculatory duct has undergone a simple morphological divergence. In order to determine whether correlated changes in GLD expression had occurred, GLD activity during the pupal and adult stages was determined for several Drosophila species. It was found that virtually all of the species exhibit pupal GLD activity, whereas only those species with an expanded ejaculatory duct express male-limited GLD. The results of interspecific genital imaginal disc transplantation experiments indicate that the expanded morphology and GLD expression do not require any species- or sex-specific diffusible factors. An apparent regulatory polymorphism exists within the D. takahashii species with respect to male-limited GLD expression.

Animals↗

Coevolution of the vertebrate integrin alpha- and beta-chain genes.

The integrin receptors are heterodimers whose alpha and beta subunits are encoded by separate, evolutionarily unrelated multigene families. Phylogenetic analysis of DNA sequences from these two gene families showed that they have not always evolved in a parallel fashion. The integrin alpha chains that can form heterodimers with beta 1 do not constitute a monophyletic group, nor do the beta chains which can form heterodimers with alpha V. On the other hand, the vertebrate alpha chains associating with beta 2 are a monophyletic group. In the metal cation-binding region of the alpha chain, an exon exchange took place between human alpha M and alpha X approximately 40-50 Mya, homogenizing this functionally important region in these two alpha chains. When integrin beta chains of different functional classes are compared, nonsynonymous (amino acid altering) nucleotide substitutions that alter amino acid residue charge in the central region of the molecule occur at a rate significantly higher than that expected under random replacement. By contrast, when closely related beta 1 chains are compared, residue charge is conserved in this region. These results pinpoint the central region as a focus of functional divergence among integrin beta chains, perhaps relating to the ability of each beta integrin class to associate with a specific array of alpha integrins. Furthermore, they imply that positive, directional selection on this region has occurred in the evolution of the integrin beta-chain gene family.

Animals↗

Predator-prey coevolution: Australian native bees avoid their spider predators.

Australian crab spiders Thomisus spectabilis manipulate visual flower signals to lure introduced Apis mellifera. We gave Australian native bees, Austroplebia australis, the choice between two white daisies, Chrysanthemum frutescens, one of them occupied by a crab spider. The colour contrast between flowers and spiders affected the behaviour of native bees. Native bees approached spider-occupied flowers more frequently. However, native bees avoided flowers occupied by spiders and landed on vacant flowers more frequently. In contrast to honeybees that did not coevolve with T. spectabilis, Australian native bees show an anti-predatory response to avoid flowers occupied by this predator.

Animals↗

Coevolution of vocal communication and sociality in primates.

Understanding the rules that link communication and social behaviour is an essential prerequisite for discerning how a communication system as complex as human language might have evolved. The comparative method offers a powerful tool for investigating the nature of these rules, since it provides a means to examine relationships between changes in communication abilities and changes in key aspects of social behaviour over evolutionary time. Here we present empirical evidence from phylogenetically controlled analyses indicating that evolutionary increases in the size of the vocal repertoire among non-human primate species were associated with increases in both group size and time spent grooming (our measure of extent of social bonding).

Animals↗

Coevolution between male ejaculates and female reproductive biology in eutherian mammals.

Among eutherian mammals, sperm competition has favoured the evolution of high sperm numbers and long spermatozoa, but it cannot account for all the variability observed. In this paper we argue that differences in female reproductive biology may also have influenced the evolution of sperm numbers as well as several other sperm traits. Sperm fertile lifespan is positively related to the interval between the onset of oestrus and ovulation, suggesting that males try to ensure that their spermatozoa will remain capable of effecting fertilization until ovulation occurs. We tentatively suggest that variation in sperm fertile lifespan may be related to differences in sperm size. The duration of capacitation is positively related to sperm fertile lifespan, suggesting that the time constraints imposed by the female have also influenced the duration of this process. When females possess long oviducts in relation to their body size, males produce relatively high sperm numbers to counteract the greater losses incurred. Contrary to our prediction, sperm size does not seem to be related to the thickness of the zona pellucida.

Animals↗

Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility.

Ebert (1994) has proposed the rule that parasites are, with few exceptions, more infective to sympatric hosts than to allopatric hosts. We test this rule using field data for schistosome infections of planorbid snails and find that, although sympatric parasite-host combinations do tend to be more compatible, there are exceptions where particular allopatric parasite-host populations are significantly more compatible. We develop a mathematical model of the dynamics of the parasite-host interaction where parasite infectivity and host susceptibility are defined by the matching of genotypes in a diploid system, The model predicts dynamic polymorphisms where parasite allele frequencies track host allele frequencies but with a lag. Because of this lag, it is possible for allopatric combinations to be more compatible than sympatric combinations. Any 'rule' that precludes this possibility is unlikely to prove robust.

Alleles↗

Host-parasite coevolution: comparative evidence for covariation of life history traits in primates and oxyurid parasites.

The environmental factors that drive the evolution of parasite life histories are mostly unknown. Given that hosts provide the principal environmental features parasites have to deal with, and given that these features (such as resource availability and immune responses) are well characterized by the life history of the host, we may expect natural selection to result in covariation between parasite and host life histories. Moreover, some parasites show a high degree of host specificity, and cladistic analyses have shown that host and parasite phylogenies can be highly congruent. These considerations suggest that parasite and host life histories may covary. The central argument in the theory of life history evolution concerns the existence of trade-offs between traits. For parasitic nematodes it has been shown that larger body sizes induce higher fecundity, but this is achieved at the expense of delayed maturity. As high adult mortality would select for reduced age at maturity, the selective benefit of increased fecundity is expressed only if adult mortality is low. Parasite adult mortality may depend on a number of factors, including host longevity. Here we tested the hypothesis concerning the positive covariation between parasite body size (which reflects parasite longevity) and host longevity. To achieve this goal, we used the association between the pinworms (Oxyuridae, Nematoda) and their primate hosts. Oxyurids are highly host specific and are supposed to be involved in a coevolutionary process with their hosts. We found that female parasite body length was positively correlated with host longevity after correcting for phylogeny and host body mass. Conversely, male parasite body length and host longevity were not correlated. These results confirm that host longevity may represent a constraint on the evolution of body size in oxyurids, at least in females. The discrepancy between female and male oxyurids is likely to depend on the particular mode of reproduction of this taxon (haplodiploidy), which should result in weak (or even null) selection pressures to an increase of body size in males.

Animals↗

Coevolution between a cockroach and its bacterial endosymbiont: a biogeographical perspective.

Cryptocercus are subsocial, xylophagous cockroaches that live in temperate forests. Like other cockroaches, Cryptocercus harbour endosymbiotic bacteria in their fat bodies. Two species of Cryptocercus occur in the palaearctic, one each in eastern Russia and south-central China. In the USA, there are five species: one in the north-west and four in the south-east. Little is known about the relationship between the Eurasian and North American Cryptocercus or the causes of the disjunct distribution. Here, a molecular phylogeny for six out of the seven Cryptocercus species and their endosymbionts is inferred in an attempt to understand the evolution and biogeography of the genus. Our analysis showed that the North American Cryptocercus are monophyletic, suggesting that a single colonization event was followed by vicariance. There was complete concordance between the host and endosymbiont phylogenetic trees. Divergence estimates based on endosymbiont DNA sequences suggested that the palaearctic and nearctic Cryptocercus diverged 70-115 million years (Myr) ago and the eastern- and western-USA species diverged 53-88 Myr ago. These divergence estimates were correlated with biogeographical events, and a hypothesis is presented to explain the current distribution of Cryptocercus. Our findings suggest that Cryptocercus has had a long evolutionary history, dating back to the Jurassic.

Animals↗

The coevolution of warning signals.

It has long been recognized that defended prey tend to be conspicuous. Current theories suggest that the association ('aposematism') has arisen because predators more readily learn to avoid attacking defended phenotypes when they are conspicuous. In this paper, I consider why such psychology has evolved. In particular, I argue that aposematism may have evolved not because of an independent and pre-existing receiver bias, but because the conspicuousness of a prey item provides a reliable indicator of its likelihood of being defended. To develop my case I consider how warning signals might coevolve in a system containing a number of predators, whose foraging behaviour is also subject to selection. In these cases, models readily show that the greater the conspicuousness of a novel prey item, the more likely that it has been encountered by other predators and survived. As a consequence, naive predators should be less likely to attack highly conspicuous novel prey on encounter, or at least more inclined to attack them cautiously. This adaptive predator behaviour will greatly facilitate the spread of aposematic phenotypes from extreme rarity, which in turn will enhance selection for forms of predator behaviour under which aposematism will coevolve even more readily.

Animals↗

Coevolution of slow-fast populations: evolutionary sliding, evolutionary pseudo-equilibria and complex Red Queen dynamics.

We study the interplay of ecological and evolutionary dynamics in communities composed of populations with contrasting time-scales. In such communities, genetic variation of individual traits can cause population transitions between stationary and cyclic ecological regimes, hence abrupt variations in fitness. Such abrupt variations raise ridges in the adaptive landscape, where the populations are poised between equilibrium and cyclic coexistence and along which evolutionary trajectories can remain sliding for long times or halt at special points called evolutionary pseudo-equilibria. These novel phenomena should be generic to all systems in which ecological interactions cause fitness to vary discontinuously. They are demonstrated by the analysis of a predator-prey community, with one adaptive trait for each population. The eco-evolutionary dynamics of the system show a number of other distinctive features, including evolutionary extinction and two forms of Red Queen dynamics. One of them is characterized by intermittent bouts of cyclic oscillations of the two populations.

Adaptation, Physiological↗

Slow coevolution of a viral pathogen and its diploid host.

We study a population exposed to a lethal infectious disease. Host response is carried at one locus with two alleles while the pathogen occurs in two variants. Based on an SI-type epidemic model we derive explicit equations for the dynamics of each genotype. By assuming small variations in both host and disease, we obtain a separation in time scales between epidemic and evolutionary processes. This allows us to describe explicitly the changes in host and disease gene frequencies. The resulting model has a rich behaviour including multiple stable states and oscillations. However, in the oscillatory situation the model is degenerate excluding the possibility of limit cycles. We show that the degeneracy can only be removed by frequency dependent selection in the pathogen, for example by including direct interaction of virus in a free-living stage. The qualitative conclusions extend to an SIR-type epidemic model, where recovery with immunity from the disease is possible.

Biological Evolution↗

The coevolution of human fertility and wealth inheritance strategies.

Life history theory concerns the scheduling of births and the level of parental investment in each offspring. In most human societies the inheritance of wealth is an important part of parental investment. Patterns of wealth inheritance and other reproductive decisions, such as family size, would be expected to influence each other. Here I present an adaptive model of human reproductive decision-making, using a state-dependent dynamic model. Two decisions made by parents are considered: when to have another baby, and thus the pattern of reproduction through life; and how to allocate resources between children at the end of the parents' life. Optimal decision rules are those that maximize the number of grandchildren. Decisions are assumed to depend on the state of the parent, which is described at any time by two variables: number of living sons, and wealth. The dynamics of the model are based on a traditional African pastoralist system, but it is general enough to approximate to any means of subsistence where an increase in the amount of wealth owned increases the capacity for future production of resources. The model is used to show that, in the unpredictable environment of a traditional pastoralist society, high fertility and a biasing of wealth inheritance to a small number of children are frequently optimal. Most such societies are now undergoing a transition to lower fertility, known as the demographic transition. The effects on fertility and wealth inheritance strategies of reducing mortality risks, reducing the unpredictability of the environment and increasing the costs of raising children are explored. Reducing mortality has little effect on completed family sizes of living children or on the wealth they inherit. Increasing the costs of raising children decreases optimal fertility and increases the inheritance left to each child at each level of wealth, and has the potential to reduce fertility to very low levels. The results offer an explanation for why wealthy families are frequently also those with the smallest number of children in heterogeneous, post-transition societies.

Africa↗

Coevolution of virulent virus and resistant cells as a mechanism of persistence of herpes simplex virus type 1 in a human T lymphoblastoid cell line.

Infection of the lymphoblastoid CEM cell line with herpes simplex virus (HSV) type 1 results in a persistent infection with production of infectious virus. Evidence suggests that the persistent infection was not maintained by interferon or non-interferon-soluble antiviral inhibitors. Treatment of persistently infected cells with anti-HSV serum (termed CEMACR cells) or elevated temperature (39 degrees C) for 14 days (termed CEMTCR cells) resulted in loss of evidence of virus. HSV DNA was not detected in CEMACR or CEMTCR cells by Southern blot or in situ hybridization. The CEMACR or CEMTCR cells, however, were resistant to reinfection with homologous, parental virus (HSV0), but were susceptible to heterologous virus (vesicular stomatitis virus). Resistance to reinfection with HSV was not absolute; CEMACR or CEMTCR cells were less permissive to virus isolated from persistently infected cultures at times early in the course of infection, but were more permissive for HSV isolated at later times. Virus isolated later during persistent infection also displayed progressively increased virulence for the parental CEM cells. These results suggest that persistent infection of a human T lymphoblastoid cell line, CEM, with HSV-1 is maintained by a genetically determined cell-virus equilibrium, in which the resistance of cells and virulence of virus increase during persistence.

Animals↗