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Non-reciprocal coevolution in a fungus-gardening ant.

Symbioses are often characterized by nonrandom associations between hosts and symbionts. Hosts may obtain symbionts horizontally from the environment or vertically from a parent or sometimes use both methods. Macroevolutionary examinations of fungus-gardening ants and their fungi have shown either a 1:1 coevolution model or a 'diffuse' model between ant host and fungal symbionts. However, some of these conclusions may have been based on using relatively conservative molecular markers, which could obscure cryptic variation. The use of whole genome approaches potentially offer more power in elucidating coevolutionary history. In this study, we examined patterns of coevolution in a single species (Trachymyrmex septentrionalis) using genomic and experimental approaches. We tested whether ant-fungal specificity patterns reflected either 1:1 or diffuse models of coevolution. While we report significant co-phylogenetic signal among intraspecific ant host and fungal symbiont lineages, we found evidence of 1:1 coevolution in some lineages and diffuse in others. These conclusions were supported by the results of experiments where newly mated T. septentrionalis queens were forced to grow novel fungi that suggested that not all fungi are equivalent symbionts and would require specialized hosts. Thus, within a single ant species, there is a mixed support for both models.

Animals

Inter-genomic sexual conflict drives antagonistic coevolution in harvester ants.

The reproductive interests of males and females are not always aligned, leading to sexual conflict over parental investment, rate of reproduction and mate choice. Traits that increase the genetic interests of one sex often occur at the expense of the other, selecting for counter-adaptations leading to antagonistic coevolution. Reproductive conflict is not limited to intraspecific interactions; interspecific hybridization can produce pronounced sexual conflict between males and females of different species, but it is unclear whether such conflict can drive sexually antagonistic coevolution between reproductively isolated genomes. We tested for hybridization-driven sexually antagonistic adaptations in queens and males of the socially hybridogenetic 'J' lineages of Pogonomyrmex harvester ants, whose mating system promotes hybridization in queens but selects against it in males. We conducted no-choice mating assays to compare patterns of mating behaviour and sperm transfer between inter- and intra-lineage pairings. There was no evidence for mate discrimination on the basis of pair type, and the total quantity of sperm transferred did not differ between intra- and inter-lineage pairs; however, further dissection of the sperm transfer process into distinct mechanistic components revealed significant, and opposing, cryptic manipulation of copulatory investment by both sexes. Males of both lineages increased their rate of sperm transfer to high-fitness intra-lineage mates, with a stronger response in the rarer lineage for whom mating mistakes are the most likely. By contrast, the total duration of copulation for intra-lineage mating pairs was significantly shorter than for inter-lineage crosses, suggesting that queens respond to prevent excessive sperm loading by prematurely terminating copulation. These findings demonstrate that sexual conflict can lead to antagonistic coevolution in both intra-genomic and inter-genomic contexts. Indeed, the resolution of sexual conflict may be a key determinant of the long-term evolutionary potential of host-dependent reproductive strategies, counteracting the inherent instabilities arising from such systems.

Animals

Coevolution: a history of the macroevolutionary approach to studying host-parasite associations.

The year 1991 marked 100 yr of coevolution research. I have reviewed the first 90 yr of this history. Three chronological phases are apparent: recognition of predictable associations among hosts and their parasites; search for patterns of association and their underlying causes, emphasizing either correlated biogeographic patterns or correlated phylogenies; and development of objective and repeatable methodologies for reconstructing and interpreting these patterns of association. Von Ihering, an outspoken anti-Darwinian, was undoubtedly the first to recognize and make use of predictable host-parasite associations. Kellogg and Fahrenholz, however, had more profound influence on subsequent generations, but in different directions. Kellogg attempted to meld natural selection with speciation by isolation. He also considered host specificity a component of coevolution, important but variable. His work laid the foundation for future research concentrated on biogeographic interpretations of host-parasite relationships. This emphasis and Metcalf's failed attempts to provide adequate mechanisms for reconstructing phylogenies reduced the biogeographic approach to an empirical research program in the hands of Manter. Fahrenholz, on the other hand, exposed to a strong anti-Darwinian sentiment, emphasized the importance of strict host specificity. This led to Eichler's formulation of the first 3 coevolutionary rules and the conclusion that host specificity was not a component but the cause of coevolution and ultimately the tautology inherent in the phylogenetic approach. All had to rely on 1 assumption, that host and parasite phylogenies were reflected in the taxonomic hierarchy. Hennig criticized this assumption and provided a method whereby phylogenies are reconstructed independently. Brooks melded this new phylogenetic method (cladistics) with an equally new biogeographic method (vicariance biogeography), providing the foundations for the modern macroevolutionary approach to studying host-parasite associations.

Animals

Evidence for cis- and trans-acting element coevolution of the 2-microns circle genome in Saccharomyces cerevisiae.

We compared the DNA sequence of the yeast 2-microns plasmid cis-acting STB and transacting REP1 partition loci of laboratory haploid and industrial amphiploid strains. Several industrial strains had a unique STB sequence (type 1) sharing only 70% homology with laboratory STB (type 2). Type 1 plasmids had a REP1 protein with 6-10% amino acid substitutions when compared to REP1 of type 2 plasmids. All 2-microns variants that shared a similar STB consensus sequence exhibited a high degree of REP1 nucleotide and amino acid sequence conservation. These observations suggest molecular coevolution of trans-acting elements with cognate target DNA structure. Based on DNA sequencing and Southern hybridization analyses, we classified 2-microns variants into two main evolutionary lineages that differ at STB as well as REP1 loci. The role of molecular coevolution in yeast intra- and interspecies plasmid evolution was discussed.

Amino Acid Sequence

Time required for gene frequency change in a deterministic model of gene-culture coevolution, with special reference to the lactose absorption problem.

The time required for gene frequency change under natural selection in a deterministic model of gene-culture coevolution is investigated. A discrete generations model is formulated, and its continuous time approximation is derived. In passing to the continuous time limit, it is assumed that the frequency of the culturally transmitted trait does not change under oblique (between generations) transmission. The system of ordinary differential equations thus obtained are solved, and the dependence on the parameters of horizontal (within generations) transmission and natural selection is examined. The time required is found to be substantially longer when the determination of a phenotypic difference subject to natural selection is partly cultural rather than completely genetic. The predictions are relevant to the possibility of the coevolution of lactose absorbers and milk drinkers in some human populations. Alternative hypotheses are briefly discussed in the light of the theoretical results.

Biological Evolution

On the relationships between the genetic code coevolution hypothesis and the physicochemical hypothesis.

This paper analyzes the relationships between the genetic code coevolution hypothesis and the physicochemical hypothesis by means of a comparative study of the precursor-product amino acid pairs on which the former hypothesis is based. Even if the coevolution between the biosynthetic relationships of amino acids and the organization of the genetic code is not questioned in this paper, the results and the arguments used lead us to believe that the selective pressures considered essential by the physicochemical postulates, played a more active role than that of the precursor-product relationships in defining the allocation of these amino acids in the genetic code. It is furthermore pointed out that the two evolutionary hypothesis might be aspects of the same selective pressure, and thus difficult to differentiate.

Amino Acids

Illuminating the coevolution of photosynthesis and Bacteria.

Life harnessing light energy transformed the relationship between biology and Earth-bringing a massive flux of organic carbon and oxidants to Earth's surface that gave way to today's organotrophy- and respiration-dominated biosphere. However, our understanding of how life drove this transition has largely relied on the geological record; much remains unresolved due to the complexity and paucity of the genetic record tied to photosynthesis. Here, through holistic phylogenetic comparison of the bacterial domain and all photosynthetic machinery (totally spanning >10,000 genomes), we identify evolutionary congruence between three independent biological systems-bacteria, (bacterio)chlorophyll-mediated light metabolism (chlorophototrophy), and carbon fixation-and uncover their intertwined history. Our analyses uniformly mapped progenitors of extant light-metabolizing machinery (reaction centers, [bacterio]chlorophyll synthases, and magnesium-chelatases) and enzymes facilitating the Calvin-Benson-Bassham cycle (form I RuBisCO and phosphoribulokinase) to the same ancient Terrabacteria organism near the base of the bacterial domain. These phylogenies consistently showed that extant phototrophs ultimately derived light metabolism from this bacterium, the last phototroph common ancestor (LPCA). LPCA was a non-oxygen-generating (anoxygenic) phototroph that already possessed carbon fixation and two reaction centers, a type I analogous to extant forms and a primitive type II. Analyses also indicate chlorophototrophy originated before LPCA. We further reconstructed evolution of chlorophototrophs/chlorophototrophy post-LPCA, including vertical inheritance in Terrabacteria, the rise of oxygen-generating chlorophototrophy in one descendant branch near the Great Oxidation Event, and subsequent emergence of Cyanobacteria. These collectively unveil a detailed view of the coevolution of light metabolism and Bacteria having clear congruence with the geological record.

Photosynthesis

Domestication as gene-culture coevolution.

Human preferences can shape the genetic evolution of other species via conservation practices, public health actions, and domestication. While the dynamics of domestication have been explored in depth through empirical and theoretical analyses, few studies have analyzed models for the coevolution of human cultural preferences with the genetics of a domesticate population. Humans shape the fitness landscape of domesticate populations both intentionally and unconsciously, by selecting for desirable traits and modifying environments; in turn, changes in domesticate phenotypes can affect the cultural preferences in the domesticator population. We present a model for the dynamics of domestication which includes interactions between genetic evolution, cultural transmission, and selective pressures. The model includes forms of selection due to culturally transmitted domesticator preferences that can affect the dynamics of domesticate genetic variants, which then affect the dynamics of domesticators. Equilibria with simultaneous genetic and cultural polymorphisms may exist, and may occur under apparent heterozygote disadvantage in the domesticate. Stable quasiperiodic cycles in both domesticates and domesticators are also possible.

Humans

Genome canalization: the coevolution of transposable and interspersed repetitive elements with single copy DNA.

Transposable and interspersed repetitive elements (TIREs) are ubiquitous features of both prokaryotic and eukaryotic genomes. However, controversy has arisen as to whether these sequences represent useless 'selfish' DNA elements, with no cellular function, as opposed to useful genetic units. In this review, we selected two insect species, the Dipteran Drosophila and the Lepidopteran Bombyx mori (the silkmoth), in an attempt to resolve this debate. These two species were selected on the basis of the special interest that our laboratory has had over the years in Bombyx with its well known molecular and developmental biology, and the wealth of genetic data that exist for Drosophila. In addition, these two species represent contrasting repetitive element types and patterns of distribution. On one hand, Bombyx exhibits the short interspersion pattern in which Alu-like TIREs predominate while Drosophila possesses the long interspersion pattern in which retroviral-like TIREs are prevalent. In Bombyx, the main TIRE family is Bm-1 while the Drosophila group contains predominantly copia-like elements, non-LTR retroposons, bacterial-type retroposons and fold-back transposable elements sequences. Our analysis of the information revealed highly non-random patterns of both TIRE biology and evolution, more indicative of these sequences acting as genomic symbionts under cellular regulation rather than useless or selfish junk DNA. In addition, we extended our analysis of potential TIRE functionality to what is known from other eukaryotic systems. From this study, it became apparent that these DNA elements may have originated as innocuous or selfish sequences and then adopted functions. The mechanism for this conversion from non-functionality to specific roles is a process of coevolution between the repetitive element and other cellular DNA often times in close physical proximity. The resulting interdependence between repetitive elements and other cellular sequences restrict the number of evolutionarily successful mutational changes for a given function or cistron. This mutual limitation is what we call genome canalization. Well documented examples are discussed to support this hypothesis and a mechanistic model is presented for how such genomic canalization can occur. Also proposed are empirical studies which would support or invalidate aspects of this hypothesis.

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

Coevolution of self-fertilization and inbreeding depression. II. Symmetric overdominance in viability.

We describe the evolutionary dynamics of a modifier of selfing coevolving with a locus subject to symmetric overdominance in viability under general levels of reduction in pollination success as a consequence of self-fertilization (pollen discounting). Simple models of the evolution of breeding systems that represent inbreeding depression as a constant parameter do not admit the possibility of stable mixed mating systems involving both inbreeding and random mating. Contrary to this expectation, we find that coevolution between a modifier of selfing and a single overdominant locus situated anywhere in the genome can generate evolutionarily attracting mixed mating systems. Two forms of association between the modifier locus and the viability locus promote the evolution of outcrossing. The favored heterozygous genotype at the viability locus develops positive associations with modifier alleles that enhance outcrossing and with the heterozygous genotype at the modifier locus. Associations between outcrossing and high viability evolve immediately upon the introduction of a rare modifier allele, even in the absence of linkage.

Alleles

Models of plant-pathogen coevolution.

Plant populations are often genetically polymorphic for resistance to pathogens. The effectiveness of this resistance is limited because the pathogens are, in turn, polymorphic for virulence genes that can evade plant resistance. Theoretical models and intriguing preliminary data suggest that these plant-pathogen polymorphisms are maintained by continual cycles of coevolution within populations, combined with occasional immigration of new virulence and resistance genes from distant populations.

Biological Evolution

Ecological and genetic models of host-pathogen coevolution.

A model is presented to analyse the forces that maintain genetic polymorphism in interactions between host plants and their pathogens. Genetic variability in hosts occurs for specific resistance to different pathogen races and variability in pathogens occurs for specific virulence to different host races. The model tracks both fluctuating population sizes and changing gene frequencies. Analyses over a range of parameters show that ecological and demographic factors, such as birth and death rates, often have a more profound effect on the amount of polymorphism than genetic parameters, such as the pleiotropic costs of resistance and virulence associated with different alleles. A series of simple measures are proposed to predict the amount of genetic polymorphism expected in particular host-pathogen interactions. These measures can be used to develop and test a comparative theory of genetic polymorphism in host-pathogen coevolution.

Biological Evolution

Coevolution in structured demes.

A simple model of coevolution in a subdivided population is considered. It is shown that, when there are frequency- and density-dependent interactions in each site, the sampling variation in numbers in each local site can lead to selection both through the dispersal process and through indirect effects. The model predicts that coevolved relationships between species can result from various interactions other than direct forms of competition and predation.

Animals

Coevolution of genes and languages revisited.

In an earlier paper it was shown that linguistic families of languages spoken by a set of 38 populations associate rather strongly with an evolutionary tree of the same populations derived from genetic data. While the correlation was clearly high, there was no evaluation of statistical significance; no such test was available at the time. This gap has now been filled by adapting to this aim a procedure based on the consistency index, and the level of significance is found to be much stronger than 10(-3). Possible reasons for coevolution of strictly genetic characters and the strictly cultural linguistic system are discussed briefly. Results of this global analysis are compared with those obtained in independent local analysis.

Animals

Hybridization breaks species barriers in long-term coevolution of a cyanobacterial population.

Bacterial species often undergo rampant recombination yet maintain cohesive genomic identity. Ecological differences can generate recombination barriers between species and sustain genomic clusters in the short term. But can these forces prevent genomic mixing during long-term coevolution? Cyanobacteria in Yellowstone hot springs comprise several diverse species that have coevolved for hundreds of thousands of years, providing a rare natural experiment. By analyzing more than 300 single-cell genomes, we show that despite each species forming a distinct genomic cluster, much of the diversity within species is the result of hybridization driven by selection, which has mixed their ancestral genotypes. This widespread mixing is contrary to the prevailing view that ecological barriers can maintain cohesive bacterial species and highlights the importance of hybridization as a source of genomic diversity.

Journal Article

Genetic and environmental interactions outweigh mitonuclear coevolution for complex traits in Drosophila.

The interdependent relationship between mitochondrial and nuclear genomes is a powerful model for understanding how epistasis shapes the architecture and evolution of complex traits. Once considered a neutral marker, mitochondrial DNA variation is now recognized as critical to phenotypic evolution because of its epistatic interactions and history of coevolution with the nuclear genome. A central challenge in evolutionary genetics is to quantify the relative importance of stabilizing and directional selection shaping complex trait distributions within and among species. Both can act on interacting and/or co-evolving genes contributing to quantitative traits, but resolving their relative roles is complicated by the complex architecture of most traits. Here, we use a panel of 90 Drosophila mitonuclear genotypes to quantify the relative contributions of mitochondrial, nuclear, and environmental variation and their interactions to four metabolically demanding complex traits. We sample both within-species and between-species mitochondrial variation and observe stronger interaction effects attributable to within-species variation, consistent with stabilizing selection maintaining mitonuclear function. Additionally, culturing the flies on a mitochondrial Complex I inhibitor, rotenone, reveals significant genotype x environment (G×E and G×G×E) interaction effects, providing insight into how genetic variation can be maintained across changing environments. Our results have broader implications in medicine, where mitochondrial DNA donors with longer purifying selection histories may be safer for mitochondrial replacement therapies.

Journal Article