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Diverse evolutionary mechanisms shape the type III effector virulence factor repertoire in the plant pathogen Pseudomonas syringae.

Many gram-negative pathogenic bacteria directly translocate effector proteins into eukaryotic host cells via type III delivery systems. Type III effector proteins are determinants of virulence on susceptible plant hosts; they are also the proteins that trigger specific disease resistance in resistant plant hosts. Evolution of type III effectors is dominated by competing forces: the likely requirement for conservation of virulence function, the avoidance of host defenses, and possible adaptation to new hosts. To understand the evolutionary history of type III effectors in Pseudomonas syringae, we searched for homologs to 44 known or candidate P. syringae type III effectors and two effector chaperones. We examined 24 gene families for distribution among bacterial species, amino acid sequence diversity, and features indicative of horizontal transfer. We assessed the role of diversifying and purifying selection in the evolution of these gene families. While some P. syringae type III effectors were acquired recently, others have evolved predominantly by descent. The majority of codons in most of these genes were subjected to purifying selection, suggesting selective pressure to maintain presumed virulence function. However, members of 7 families had domains subject to diversifying selection.

Base Composition↗

Darwinian adaptation, population genetics and the streetcar theory of evolution.

This paper investigates the problem of how to conceive a robust theory of phenotypic adaptation in non-trivial models of evolutionary biology. A particular effort is made to develop a foundation of this theory in the context of n-locus population genetics. Therefore, the evolution of phenotypic traits is considered that are coded for by more than one gene. The potential for epistatic gene interactions is not a priori excluded. Furthermore, emphasis is laid on the intricacies of frequency-dependent selection. It is first discussed how strongly the scope for phenotypic adaptation is restricted by the complex nature of 'reproduction mechanics' in sexually reproducing diploid populations. This discussion shows that one can easily lose the traces of Darwinism in n-locus models of population genetics. In order to retrieve these traces, the outline of a new theory is given that I call 'streetcar theory of evolution'. This theory is based on the same models that geneticists have used in order to demonstrate substantial problems with the 'adaptationist programme'. However, these models are now analyzed differently by including thoughts about the evolutionary removal of genetic constraints. This requires consideration of a sufficiently wide range of potential mutant alleles and careful examination of what to consider as a stable state of the evolutionary process. A particular notion of stability is introduced in order to describe population states that are phenotypically stable against the effects of all mutant alleles that are to be expected in the long-run. Surprisingly, a long-term stable state can be characterized at the phenotypic level as a fitness maximum, a Nash equilibrium or an ESS. The paper presents these mathematical results and discusses - at unusual length for a mathematical journal - their fundamental role in our current understanding of evolution.

Animals↗

A protein alignment scoring system sensitive at all evolutionary distances.

Protein sequence alignments generally are constructed with the aid of a "substitution matrix" that specifies a score for aligning each pair of amino acids. Assuming a simple random protein model, it can be shown that any such matrix, when used for evaluating variable-length local alignments, is implicitly a "log-odds" matrix, with a specific probability distribution for amino acid pairs to which it is uniquely tailored. Given a model of protein evolution from which such distributions may be derived, a substitution matrix adapted to detecting relationships at any chosen evolutionary distance can be constructed. Because in a database search it generally is not known a priori what evolutionary distances will characterize the similarities found, it is necessary to employ an appropriate range of matrices in order not to overlook potential homologies. This paper formalizes this concept by defining a scoring system that is sensitive at all detectable evolutionary distances. The statistical behavior of this scoring system is analyzed, and it is shown that for a typical protein database search, estimating the originally unknown evolutionary distance appropriate to each alignment costs slightly over two bits of information, or somewhat less than a factor of five in statistical significance. A much greater cost may be incurred, however, if only a single substitution matrix, corresponding to the wrong evolutionary distance, is employed.

Algorithms↗

Gene flow maintains a large genetic difference in clutch size at a small spatial scale.

Understanding the capacity of natural populations to adapt to their local environment is a central topic in evolutionary biology. Phenotypic differences between populations may have a genetic basis, but showing that they reflect different adaptive optima requires the quantification of both gene flow and selection. Good empirical data are rare. Using data on a spatially structured island population of great tits (Parus major), we show here that a persistent difference in mean clutch size between two subpopulations only a few kilometres apart has a major genetic component. We also show that immigrants from outside the island carry genes for large clutches. But gene flow into one subpopulation is low, as a result of a low immigration rate together with strong selection against immigrant genes. This has allowed for adaptation to the island environment and the maintenance of small clutches. In the other area, however, higher gene flow prevents local adaptation and maintains larger clutches. We show that the observed small-scale genetic difference in clutch size is not due to divergent selection on the island, but to different levels of gene flow from outside the island. Our findings illustrate the large effect of immigration on the evolution of local adaptations and on genetic population structure.

Animal Migration↗

Dynamics of metal adaptation in riverine chironomids.

The ability of the non-biting midge Chironomus riparius to survive and reproduce in metal polluted lowland rivers facilitates the opportunity to study micro-evolutionary processes in situ. However, due to larval drift, adapted midge populations are subject to regular immigration of non-adapted specimens from clean upstream river reaches. To examine the influence of non-adapted genes in adapted midge populations on the level of metal adaptation, an upstream and downstream chironomid population were crossbred on eight separate occasions in the laboratory to mimic gene flow. Several life-history characteristics, indicating adaptation to metals, were followed seasonally in the parental strains as well as in the reciprocal crossings. Such crossings were done over a 14-month period and maternal effects were found to be absent, indicating a major genetic component for the increased metal tolerance in the exposed midge populations. Furthermore, results confirmed the presence of adaptation to metals in exposed chironomids. However, a rapid loss of metal adaptation in the first generation hybrid offspring was clearly demonstrated. Consequently, the large temporal variation in metal adaptation in midge populations from the river can be explained by the earlier reported seasonal variations in selection pressure and immigration rates from non-adapted sub-populations.

Adaptation, Physiological↗

Molecular evolutionary relationships between partulid land snails of the Pacific.

Adaptive radiation of partulid land snails in the tropical Pacific has produced an extraordinary array of distinctive morphological, ecological and behavioural types. Here we use part of the nuclear ribosomal RNA gene cluster to investigate the relationships within and between the three partulid genera, Partula, Samoana and Eua. The genera cluster separately, with Samoana and Partula forming monophyletic groups. With one exception, the molecular data generally support the previous generic classification based on genital morphology, even in species that show a number of characteristics otherwise atypical of the genus. Convergent evolution explains morphological similarities between members of different genera. The phylogeny suggests that Samoana has colonized the Pacific from west to east, originating in the area where Eua, believed to be the most ancient partulid genus, is found. An unexplained anomaly is the reported occurrence of a single species of Samoana in the Mariana Islands of the western Pacific. The genus Partula has a disjunct distribution, encompassing islands both to the east and west of the range occupied by Eua. Partula seems to have spread both eastward and westward after the splitting of the Partula lineage.

Animals↗

Linking biogeography to physiology: Evolutionary and acclimatory adjustments of thermal limits.

Temperature-adaptive physiological variation plays important roles in latitudinal biogeographic patterning and in setting vertical distributions along subtidal-to-intertidal gradients in coastal marine ecosystems. Comparisons of congeneric marine invertebrates reveal that the most warm-adapted species may live closer to their thermal tolerance limits and have lower abilities to increase heat tolerance through acclimation than more cold-adapted species. In crabs and snails, heart function may be of critical importance in establishing thermal tolerance limits. Temperature-mediated shifts in gene expression may be critical in thermal acclimation. Transcriptional changes, monitored using cDNA microarrays, have been shown to differ between steady-state thermal acclimation and diurnal temperature cycling in a eurythermal teleost fish (Austrofundulus limnaeus). In stenothermal Antarctic notothenioid fish, losses in capacity for temperature-mediated gene expression, including the absence of a heat-shock response, may reduce the abilities of these species to acclimate to increased temperatures. Differences among species in thermal tolerance limits and in the capacities to adjust these limits may determine how organisms are affected by climate change.

Journal Article↗

Parallel adaptive origins of digestive RNases in Asian and African leaf monkeys.

Similar morphological or physiological changes occurring in multiple evolutionary lineages are not uncommon. Such parallel changes are believed to be adaptive, because a complex character is unlikely to originate more than once by chance. However, the occurrence of adaptive parallel amino acid substitutions is debated. Here I propose four requirements for establishing adaptive parallel evolution at the protein sequence level and use these criteria to demonstrate such a case. I report that the gene encoding pancreatic ribonuclease was duplicated independently in Asian and African leaf-eating monkeys. Statistical analyses of DNA sequences, functional assays of reconstructed ancestral proteins and site-directed mutagenesis show that the new genes acquired enhanced digestive efficiencies through parallel amino acid replacements driven by darwinian selection. They also lost a non-digestive function independently, under a relaxed selective constraint. These results demonstrate that despite the overall stochasticity, even molecular evolution has a certain degree of repeatability and predictability under the pressures of natural selection.

Adaptation, Physiological↗

Correlational selection and the evolution of genomic architecture.

We review and discuss the importance of correlational selection (selection for optimal character combinations) in natural populations. If two or more traits subject to multivariate selection are heritable, correlational selection builds favourable genetic correlations through the formation of linkage disequilibrium at underlying loci governing the traits. However, linkage disequilibria built up by correlational selection are expected to decay rapidly (ie, within a few generations), unless correlational selection is strong and chronic. We argue that frequency-dependent biotic interactions that have 'Red Queen dynamics' (eg, host-parasite interactions, predator-prey relationships or intraspecific arms races) often fuel chronic correlational selection, which is strong enough to maintain adaptive genetic correlations of the kind we describe. We illustrate these processes and phenomena using empirical examples from various plant and animal systems, including our own recent work on the evolutionary dynamics of a heritable throat colour polymorphism in the side-blotched lizard Uta stansburiana. In particular, male and female colour morphs of side-blotched lizards cycle on five- and two-generation (year) timescales under the force of strong frequency-dependent selection. Each morph refines the other morph in a Red Queen dynamic. Strong correlational selection gradients among life history, immunological and morphological traits shape the genetic correlations of the side-blotched lizard polymorphism. We discuss the broader evolutionary consequences of the buildup of co-adapted trait complexes within species, such as the implications for speciation processes.

Animals↗

What we have also learned: adaptive speciation is theoretically plausible.

A recent Perspectives article by Gavrilets (2003) on the theory of speciation ignored advances in understanding processes of adaptive speciation, in which the splitting of lineages is an adaptation caused by frequency-dependent selection. Adaptive, or sympatric, speciation has been modeled since the 1960s, but the large amount of attention from both empirical and theoretical biologists that adaptive speciation has received in recent years goes far beyond what was described in Gavrilets' paper. Due to conceptual advances based on the theory of adaptive dynamics, adaptive speciation has emerged as a theoretically plausible evolutionary process that can occur in many different ecological settings.

Adaptation, Biological↗

Mapping Species Birth Across the Recombination Landscapes of Marine Snails.

Understanding the drivers of heterogeneous genomic divergence is essential for uncovering the mechanisms that generate and constrain biodiversity. The extent to which adaptation and speciation are facilitated by reorganisation of the recombination landscape remains untested in many systems. Marine ecosystems, with their dynamic and fluid habitats, offer a compelling context to investigate genomic divergence. In this study, we mapped genomic divergence and selection across recombination landscapes of parapatric marine snail sister species that we show have recently undergone secondary contact. Regions of reduced recombination were enriched for genes exhibiting signatures of negative selection, whereas regions of high recombination were associated with genes under putative positive selection. Notably, the recombination landscape of the population in parapatry of one species (Scurria viridula) differs markedly from that of the other population within this same species, highlighting the role of introgression in reshaping recombination landscapes. In the other species (Scurria zebrina), conservation of the recombination landscape and divergent selection among populations suggest trapping of beneficial allele combinations in regions of low recombination maintains the identity of this species. Among species, signals of divergence with gene flow consistently cluster within specific genomic regions characterised by high recombination rate variation among the populations of S. viridula. These results challenge traditional theoretical expectations of recombination evolution by showing that the causes of genomic divergence can be population-specific. This study demonstrates that recombination landscapes are key modulators of genomic divergence, with contemporary evolutionary shifts that could enable populations to adapt to distinct environments. Our findings provide new insights into the interplay between recombination, selection, and gene flow during speciation, underscoring the complexity of evolutionary trajectories in marine systems.

Genetic Introgression↗

Geographic variation in acid stress tolerance of the moor frog, Rana arvalis. I. Local adaptation.

Spatially varying directional selection together with restricted gene flow among populations is expected to lead to local adaptation. One environmental factor that potentially causes strong directional selection, but is little explored in evolutionary terms, is naturally and anthropogenically induced acidity. We studied local adaptation to acidity in four Swedish populations (two originating from areas that have suffered from severe anthropogenic acidification during the 1900s and two from areas which have remained neutral due to higher buffering capacity) of the moor frog Rana arvalis in a laboratory experiment by investigating whether differences in acid tolerance correspond to population origin. Embryos were raised from fertilization to hatching at three different pH levels (pH 4.0, 4.25 and 7.5), corresponding to levels experienced by these populations in nature, and acid stress tolerance was measured in terms of embryonic survival, hatchling size, and age. Evidence for local adaptation in all of these traits was found, the acid origin embryos having higher survival and less impaired growth performance under acid conditions than the neutral origin embryos. Our estimated rates of divergence (0.007-0.102 haldanes) suggest a rapid adaptation process in response to anthropogenic environmental change, and that the different traits have evolved at relatively similar rates.

Adaptation, Physiological↗

Relationship between diet and helminths in Gallotia caesaris (Sauria: Lacertidae).

Diet and helminth fauna were analysed in Gallotia caesaris, a small lacertid lizard endemic to El Hierro (Canary Islands, Spain) in order to study the evolutionary and functional relationships between the two traits. This species is omnivorous but consumed a high proportion (82.13%) of plant matter including not only seeds but also leaves and other vegetative parts. Helminth fauna included many helminth species typical of herbivorous reptiles. Both herbivory and helminth presence were higher than expected for a lizard of its size. Comparison with other lacertids suggests that both traits result from an adaptation to insular conditions but that some "evolutionary time" to develop them is needed. Canarian Gallotia lizards, a separate lineage evolving for a long time in insularity, constitutes the most advanced lacertid group in this way. Nevertheless, results for G. caesaris indicate that helminth fauna also changes seasonally tracking variation in diet (and herbivory) throughout the year, which suggests a dynamic interaction between diet and helminth parasites.

Analysis of Variance↗

Prediction of local convergent shifts in evolutionary rates with phyloConverge.

MOTIVATION: Convergence analysis can characterize genetic elements underlying morphological adaptations. However, its performance on regulatory elements is limited due to their modular composition of transcription factor motifs, which have rapid turnover and experience different evolutionary pressures. RESULTS: We introduce phyloConverge, a phylogenetic method that performs scalable, fine-grained local convergence analysis of genomic elements at flexible length scales. Using a benchmarking case of convergent subterranean mammal adaptation, phyloConverge identifies rate-accelerated conserved noncoding elements (CNEs) with high specificity and statistical robustness relative to competing methods. From CNE-level scoring, we detect the convergent regression of entire CNE units and highlight the contrast that subterranean-associated coding region regression is highly specific to ocular functions, whereas regulatory element regression is enriched for accompanying neuronal phenotypes and other developmental processes. From transcription factor motif-level scoring, we dissect elements into subregions with uneven convergence signals and demonstrate the modular adaptation of CNEs with high functional specificity. Finally, we demonstrate phyloConverge's scalability to perform high-resolution convergence analysis genome-wide. AVAILABILITY AND IMPLEMENTATION: phyloConverge is available at https://github.com/ECSaputra/phyloConverge.

Evolution, Molecular↗

Fructophilic lactic acid bacteria as a window into multi-scale convergent evolution.

Fructophilic lactic acid bacteria (FLAB) are a group of lactic acid bacteria with unique growth characteristics, that is, poor growth on glucose. Their growth is enhanced in the presence of fructose or external electron acceptors. These organisms inhabit fructose-rich environments such as flowers, fruits, and pollinating insects, particularly honey bees. Apilactobacillus spp. and Fructobacillus spp. are representatives of FLAB, although they belong to phylogenetically distant clades. These organisms commonly possess markedly small genomes with a low number of coding DNA sequences. Furthermore, their genomes are characterized by a markedly reduced number of genes involved in carbohydrate transport and metabolism. Genome reduction in FLAB reflects convergent adaptation to fructose-rich environments rather than general genome streamlining. The two distinct FLAB genera, Fructobacillus and Apilactobacillus, independently lost more than 100 genes in statistically similar orders. In contrast, genes involved in carbohydrate and amino acid metabolism exhibited reversed orders of loss between the two genera. Furthermore, FLAB genomes lack an intact bifunctional alcohol/aldehyde dehydrogenase gene (adhE), which causes their poor growth on glucose. A comparative genomic study suggested the evolutionary process underlying adhE gene decay during adaptation to the fructose-rich environments, including pollinating insects. In conclusion, FLAB represent a unique example of habitat-driven convergent reductive evolution that can be investigated across multiple biological scales - from individual genes to whole genomes - in the diverse LAB group with a wide range of habitats, and partially share the fructophilic evolution with eukaryotic yeasts found in fructose-rich habitats.

Fructose↗

The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins.

We propose that a key change in the evolution of hominids from the last common ancestor shared with chimpanzees was the substitution of plant underground storage organs (USOs) for herbaceous vegetation as fallback foods. Four kinds of evidence support this hypothesis: (1) dental and masticatory adaptations of hominids in comparison with the African apes; (2) changes in australopith dentition in the fossil record; (3) paleoecological evidence for the expansion of USO-rich habitats in the late Miocene; and (4) the co-occurrence of hominid fossils with root-eating rodents. We suggest that some of the patterning in the early hominid fossil record, such as the existence of gracile and robust australopiths, may be understood in reference to this adaptive shift in the use of fallback foods. Our hypothesis implicates fallback foods as a critical limiting factor with far-reaching evolutionary effects. This complements the more common focus on adaptations to preferred foods, such as fruit and meat, in hominid evolution.

Adaptation, Biological↗

Schizophrenia-an evolutionary enigma?

The term 'schizophrenia' refers to a group of disorders that have been described in every human culture. Two apparently well established findings have corroborated the need for an evolutionary explanation of these disorders: (1) cross-culturally stable incidence rates and (2) decreased fecundity of the affected individuals. The rationale behind this relates to the evolutionary paradox that susceptibility genes for schizophrenia are obviously preserved in the human genepool, despite fundamental reproductive disadvantages associated with the disorders. Some researchers have therefore proposed that a compensatory advantage must exist in people who are carriers of these genes or in their first-degree relatives. Such advantages were hypothesised to be outside the brain (e.g. greater resistance against toxins or infectious diseases), or within the social domain (e.g. schizotypal shamans, creativity). More specifically, T.J. Crow has suggested an evolutionary theory of schizophrenia that relates the disorders to an extreme of variation of hemispheric specialisation and the evolution of language due to a single gene mutation located on homologous regions of the sex chromosomes. None of the evolutionary scenarios does, however, fully account for the diversity of the symptomatology, nor does any one hypothesis acknowledge the objection that the mere prevalence of a disorder must not be confused with adaptation. In the present article, I therefore discuss the evolutionary hypotheses of schizophrenia, arguing that a symptom-based approach to psychotic disorders in evolutionary perspective may improve upon the existing models of schizophrenia.

Adaptation, Biological↗

Engineering of a cold-adapted protease by sequential random mutagenesis and a screening system.

A cold-adapted protease subtilisin was successfully isolated by evolutionary engineering based on sequential in vitro random mutagenesis and an improved method of screening (H. Kano, S. Taguchi, and H. Momose, Appl. Microbiol. Biotechnol. 47:46-51, 1997). The mutant subtilisin, termed m-63, exhibited a catalytic efficiency (expressed as the kcat/Km value) 100% higher than that of the wild type at 10 degrees C when N-succinyl-L-Ala-L-Ala-L-Pro-L-Phe-p-nitroanilide was used as a synthetic substrate. This cold adaptation was achieved with three mutations, Val to Ile at position 72 (V72I), Ala to Thr at position 92 (A92T), and Gly to Asp at position 131 (G131D), and it was found that an increase in substrate affinity (i.e., a decreased Km value) was mostly responsible for the increased activity. Analysis of kinetic parameters revealed that the V72I mutation contributed negatively to the activity but that the other two mutations, A92T and G131D, overcame the negative contribution to confer the 100% increase in activity. Besides suppression of the activity-negative mutation (V72I) by A92T and G131D, suppression of structural stability was observed in measurements of activity retention at 60 degrees C and circular dichroism spectra at 10 degrees C.

Cold Temperature↗