Experimental evidence that source genetic variation drives pathogen emergence

A pathogen can readily mutate to infect new host types, but this does not guarantee successful establishment in the new habitat. What factors, then, dictate emergence success? One possibility is that the pathogen population cannot sustain itself on the new host type (i.e. host is a sink), but migration from a source population allows adaptive sustainability and eventual emergence by delivering beneficial mutations sampled from the source''s standing genetic variation. This idea is relevant regardless of whether the sink host is truly novel (host shift) or whether the sink is an existing or related, similar host population thriving under conditions unfavourable to pathogen persistence (range expansion). We predicted that sink adaptation should occur faster under range expansion than during a host shift owing to the effects of source genetic variation on pathogen adaptability in the sink. Under range expansion, source migration should benefit emergence in the sink because selection acting on source and sink populations is likely to be congruent. By contrast, during host shifts, source migration is likely to disrupt emergence in the sink owing to uncorrelated selection or performance tradeoffs across host types. We tested this hypothesis by evolving bacteriophage populations on novel host bacteria under sink conditions, while manipulating emergence via host shift versus range expansion. Controls examined sink adaptation when unevolved founding genotypes served as migrants. As predicted, adaptability was fastest under range expansion, and controls did not adapt. Large, similar and similarly timed increases in fitness were observed in the host-shift populations, despite declines in mean fitness of immigrants through time. These results suggest that source populations are the origin of mutations that drive adaptive emergence at the edge of a pathogen''s ecological or geographical range.     

Origin and maintenance of sex: the evolutionary joys of self sex

Sex is generally thought of as meiosis, conjugation, and syngamy, with the primary function of sex believed to be genetic mixing. However, conjugation does not occur with complete automixis, whereas syngamy does not occur with restitutional automixis. Self sex in the forms of automixis and autogamy does not include genetic mixing. Yet sex, including self sex, is necessary for most eukaryotic lineages. What is the purpose of sex without genetic mixing? Obligate self sex is not an evolutionary dead end, but holds the key to understanding the evolutionary origin, function, maintenance, and ubiquity of sex. We extend the rejuvenescence hypothesis that sex provides a necessary developmental reset for multicellular eukaryotes and even many unicellular eukaryotes. Sex reduces additive genetic variance of epigenetic signals, especially cytosine methylation, and of ploidy levels. Furthermore, we argue that syngamy is a modified form of meiosis that maintains ploidy and resets epigenetic signals. Epigenetic resetting is consistent with sex being induced by starvation or desiccation. Diminution of additive genetic variance is consistent with the origin and maintenance of an adaptive trait, sex, that has been present for approximately two billion years. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 707–728.     

Evolution of sexual asymmetry

Background

The clear dominance of two-gender sex in recent species is a notorious puzzle of evolutionary theory. It has at least two layers: besides the most fundamental and challenging question why sex exists at all, the other part of the problem is equally perplexing but much less studied. Why do most sexual organisms use a binary mating system? Even if sex confers an evolutionary advantage (through whatever genetic mechanism), why does it manifest that advantage in two, and exactly two, genders (or mating types)? Why not just one, and why not more than two?

Results

Assuming that sex carries an inherent fitness advantage over pure clonal multiplication, we attempt to give a feasible solution to the problem of the evolution of dimorphic sexual asymmetry as opposed to monomorphic symmetry by using a spatial (cellular automaton) model and its non-spatial (mean-field) approximation. Based on a comparison of the spatial model to the mean-field approximation we suggest that spatial population structure must have played a significant role in the evolution of mating types, due to the largely clonal (self-aggregated) spatial distribution of gamete types, which is plausible in aquatic habitats for physical reasons, and appears to facilitate the evolution of a binary mating system.

Conclusions

Under broad ecological and genetic conditions the cellular automaton predicts selective removal from the population of supposedly primitive gametes that are able to mate with their own type, whereas the non-spatial model admits coexistence of the primitive type and the mating types. Thus we offer a basically ecological solution to a theoretical problem that earlier models based on random gamete encounters had failed to resolve.

     

Chasing the Origin of Viruses: Capsid-Forming Genes as a Life-Saving Preadaptation within a Community of Early Replicators

Virus capsids mediate the transfer of viral genetic information from one cell to another, thus the origin of the first viruses arguably coincides with the origin of the viral capsid. Capsid genes are evolutionarily ancient and their emergence potentially predated even the origin of first free-living cells. But does the origin of the capsid coincide with the origin of viruses, or is it possible that capsid-like functionalities emerged before the appearance of true viral entities? We set to investigate this question by using a computational simulator comprising primitive replicators and replication parasites within a compartment matrix. We observe that systems with no horizontal gene transfer between compartments collapse due to the rapidly emerging replication parasites. However, introduction of capsid-like genes that induce the movement of randomly selected genes from one compartment to another rescues life by providing the non-parasitic replicators a mean to escape their current compartments before the emergence of replication parasites. Capsid-forming genes can mediate the establishment of a stable meta-population where parasites cause only local tragedies but cannot overtake the whole community. The long-term survival of replicators is dependent on the frequency of horizontal transfer events, as systems with either too much or too little genetic exchange are doomed to succumb to replication-parasites. This study provides a possible scenario for explaining the origin of viral capsids before the emergence of genuine viruses: in the absence of other means of horizontal gene transfer between compartments, evolution of capsid-like functionalities may have been necessary for early life to prevail.     

Ever-young sex chromosomes in European tree frogs

Non-recombining sex chromosomes are expected to undergo evolutionary decay, ending up genetically degenerated, as has happened in birds and mammals. Why are then sex chromosomes so often homomorphic in cold-blooded vertebrates? One possible explanation is a high rate of turnover events, replacing master sex-determining genes by new ones on other chromosomes. An alternative is that X-Y similarity is maintained by occasional recombination events, occurring in sex-reversed XY females. Based on mitochondrial and nuclear gene sequences, we estimated the divergence times between European tree frogs (Hyla arborea, H. intermedia, and H. molleri) to the upper Miocene, about 5.4–7.1 million years ago. Sibship analyses of microsatellite polymorphisms revealed that all three species have the same pair of sex chromosomes, with complete absence of X-Y recombination in males. Despite this, sequences of sex-linked loci show no divergence between the X and Y chromosomes. In the phylogeny, the X and Y alleles cluster according to species, not in groups of gametologs. We conclude that sex-chromosome homomorphy in these tree frogs does not result from a recent turnover but is maintained over evolutionary timescales by occasional X-Y recombination. Seemingly young sex chromosomes may thus carry old-established sex-determining genes, a result at odds with the view that sex chromosomes necessarily decay until they are replaced. This raises intriguing perspectives regarding the evolutionary dynamics of sexually antagonistic genes and the mechanisms that control X-Y recombination.     

Drosophila sex combs as a model of evolutionary innovations

The diversity of animal and plant forms is shaped by nested evolutionary innovations. Understanding the genetic and molecular changes responsible for these innovations is therefore one of the key goals of evolutionary biology. From the genetic point of view, the origin of novel traits implies the origin of new regulatory pathways to control their development. To understand how these new pathways are assembled in the course of evolution, we need model systems that combine relatively recent innovations with a powerful set of genetic and molecular tools. One such model is provided by the Drosophila sex comb—a male‐specific morphological structure that evolved in a relatively small lineage related to the model species D. melanogaster. Our extensive knowledge of sex comb development in D. melanogaster provides the basis for investigating the genetic changes responsible for sex comb origin and diversification. At the same time, sex combs can change on microevolutionary timescales and differ spectacularly among closely related species, providing opportunities for direct genetic analysis and for integrating developmental and population‐genetic approaches. Sex comb evolution is associated with the origin of novel interactions between Hox and sex determination genes. Activity of the sex determination pathway was brought under the control of the Hox code to become segment‐specific, while Hox gene expression became sexually dimorphic. At the same time, both Hox and sex determination genes were integrated into the intrasegmental spatial patterning network, and acquired new joint downstream targets. Phylogenetic analysis shows that similar sex comb morphologies evolved independently in different lineages. Convergent evolution at the phenotypic level reflects convergent changes in the expression of Hox and sex determination genes, involving both independent gains and losses of regulatory interactions. However, the downstream cell‐differentiation programs have diverged between species, and in some lineages, similar adult morphologies are produced by different morphogenetic mechanisms. These features make the sex comb an excellent model for examining not only the genetic changes responsible for its evolution, but also the cellular processes that translate DNA sequence changes into morphological diversity. The origin and diversification of sex combs provides insights into the roles of modularity, cooption, and regulatory changes in evolutionary innovations, and can serve as a model for understanding the origin of the more drastic novelties that define higher order taxa.     

How an organism dies affects the fitness of its neighbors

Programmed cell death (PCD), a genetically regulated cell suicide program, is ubiquitous in the living world. In contrast to multicellular organisms, in which cells cooperate for the good of the organism, in unicells the cell is the organism and PCD presents a fundamental evolutionary problem. Why should an organism actively kill itself as opposed to dying in a nonprogrammed way? Proposed arguments vary from PCD in unicells being maladaptive to the assumption that it is an extreme form of altruism. To test whether PCD could be beneficial to nearby cells, we induced programmed and nonprogrammed death in the unicellular green alga Chlamydomonas reinhardtii. Cellular contents liberated during non-PCD are detrimental to others, while the contents released during PCD are beneficial. The number of cells in growing cultures was used to measure fitness. Thermostability studies revealed that the beneficial effect of the PCD supernatant most likely involves simple heat-stable biomolecules. Non-PCD supernatant contains heat-sensitive molecules like cellular proteases and chlorophyll. These data indicate that the mode of death affects the origin and maintenance of PCD. The way in which an organism dies can have beneficial or deleterious effects on the fitness of its neighbors.     

Having sex,yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types

The advantage of sex has been among the most debated issues in biology. Surprisingly, the question of why sexual reproduction generally requires the combination of distinct gamete classes, such as small and large gametes, or gametes with different mating types, has been much less investigated. Why do systems with alternative gamete classes (i.e. systems with either anisogamy or mating types or both) appear even though they restrict the probability of finding a compatible mating partner? Why does the number of gamete classes vary from zero to thousands, with most often only two classes? We review here the hypotheses proposed to explain the origin, maintenance, number, and loss of gamete classes. We argue that fungi represent highly suitable models to help resolve issues related to the evolution of distinct gamete classes, because the number of mating types vary from zero to thousands across taxa, anisogamy is present or not, and because there are frequent transitions between these conditions. We review the nature and number of gamete classes in fungi, and we attempt to draw inferences from these data on the evolutionary forces responsible for their appearance, loss or maintenance, and number.     

Molecular and evolutionary analysis of a plant Y chromosome.

Plants have evolved a great diversity of sex determination systems. Among these, the XY system, also found in mammals, is one of the most exciting since it gives the opportunity to compare the evolution of sex chromosomes in two different kingdoms. Whereas genetic and molecular mechanisms controlling sex determination in drosophila and mammals, have been well studied, very little is known about such processes in plants. White campion (Silene latifolia) is an example of plant with X and Y chromosomes. What is the origin of the X and Y chromosomes? How did they evolve from a pair of autosomes? In our laboratory, we have isolated the first active genes located on a plant Y chromosome. We are using them as markers to trace the origin and evolution of sex chromosomes in the Silene genus.     

Recombination difference between sexes: a role for haploid selection

Why the autosomal recombination rate differs between female and male meiosis in most species has been a genetic enigma since the early study of meiosis. Some hypotheses have been put forward to explain this widespread phenomenon and, up to now, only one fact has emerged clearly: In species in which meiosis is achiasmate in one sex, it is the heterogametic one. This pattern, known as the Haldane-Huxley rule, is thought to be a side effect, on autosomes, of the suppression of recombination between the sex chromosomes. However, this rule does not hold for heterochiasmate species (i.e., species in which recombination is present in both sexes but varies quantitatively between sexes) and does not apply to species lacking sex chromosomes, such as hermaphroditic plants. In this paper, we show that in plants, heterochiasmy is due to a male-female difference in gametic selection and is not influenced by the presence of heteromorphic sex chromosomes. This finding provides strong empirical support in favour of a population genetic explanation for the evolution of heterochiasmy and, more broadly, for the evolution of sex and recombination.     

The impact of global climate change on genetic diversity within populations and species

Genetic diversity provides the basic substrate for evolution, yet few studies assess the impacts of global climate change (GCC) on intraspecific genetic variation. In this review, we highlight the importance of incorporating neutral and non‐neutral genetic diversity when assessing the impacts of GCC, for example, in studies that aim to predict the future distribution and fate of a species or ecological community. Specifically, we address the following questions: Why study the effects of GCC on intraspecific genetic diversity? How does GCC affect genetic diversity? How is the effect of GCC on genetic diversity currently studied? Where is potential for future research? For each of these questions, we provide a general background and highlight case studies across the animal, plant and microbial kingdoms. We further discuss how cryptic diversity can affect GCC assessments, how genetic diversity can be integrated into studies that aim to predict species' responses on GCC and how conservation efforts related to GCC can incorporate and profit from inclusion of genetic diversity assessments. We argue that studying the fate of intraspecifc genetic diversity is an indispensable and logical venture if we are to fully understand the consequences of GCC on biodiversity on all levels.     

Complex adaptive systems, aging and longevity.

Mortality and reproduction are intimately entwined in the study of aging and longevity. I apply the modern theory of complex adaptive systems (nonlinear, stochastic, dynamic methods) to questions of aging and longevity. I begin by highlighting major questions that must be answered in order to obtain a deeper understanding of aging. These are: (i) What should (in an evolutionary sense) mortality trajectories look like? (ii) Why does caloric restriction slow aging? (iii) Why does reproduction cause delayed mortality? (iv) Why does compensatory growth cause delayed mortality? I show how dynamic state variable models based on stochastic dynamic programming (Clark & Mangel, 2000) can be used to embed genetic theories of senescence (either mutation accumulation or antagonistic pleiotropy) in the somatic environment, as George Williams called for in 1957, and how they make the disposable soma theory of aging operational. Such models will allow unification of genetic and phenotypic theories of aging.     

Aurora kinases, aneuploidy and cancer, a coincidence or a real link?

As Aurora kinases are overexpressed in a large number of cancers, and ectopic expression of Aurora generates polyploid cells containing multiple centrosomes, it has been tempting to suggest that Aurora overexpression provokes genetic instability underlying the tumorigenesis. However, examination of the evidence suggests a more complex relationship. Overexpression of Aurora-A readily transforms rat-1 and NIH3T3 cells, but not primary cells, whereas overexpression of Aurora-B induces metastasis after implantation of tumors in nude mice. Why do polyploid cells containing abnormal centrosome numbers induced by Aurora not get eliminated at cell-cycle checkpoints? Does this phenotype determine the origin of cancer or does it only promote tumor progression? Would drugs against Aurora family members be of any help for cancer treatment? These and related questions are addressed in this review (which is part of the Chromosome Segregation and Aneuploidy series).     

A gene's-eye view of symbiont transmission

Symbiotic associations between species are ubiquitous, but we only poorly understand why some symbioses evolve to be mutualistic and others to be parasitic. One prominent hypothesis holds that vertical transmission of symbionts from host parents to their offspring selects for symbionts that are benign or beneficial, while horizontal transmission of symbionts among unrelated hosts selects for symbionts that are less beneficial or outright harmful. A long-standing challenge to this hypothesis, however, is the existence of selfish genetic elements (SGEs). SGEs are passed exclusively from parent to offspring and are able to spread and persist in populations despite reducing the fitness of their hosts. Here I show that SGEs are in fact consistent with the transmission mode hypothesis if one measures transmission from the perspective of host genes instead of host organisms. Both meiotic drive genes and cytoplasmic sex ratio distorters require horizontal transmission, in the form of outbred sex, to spread as parasites. Transmission from parent to offpsring does not constrain SGEs to evolve toward mutualism. The gene-centered perspective I present here is applicable to symbioses at all levels of selection and brings closer together our understandings of cooperation within and between species.     

The puzzle of the Krebs citric acid cycle: Assembling the pieces of chemically feasible reactions,and opportunism in the design of metabolic pathways during evolution

The evolutionary origin of the Krebs citric acid cycle has been for a long time a model case in the understanding of the origin and evolution of metabolic pathways: How can the emergence of such a complex pathway be explained? A number of speculative studies have been carried out that have reached the conclusion that the Krebs cycle evolved from pathways for amino acid biosynthesis, but many important questions remain open: Why and how did the full pathway emerge from there? Are other alternative routes for the same purpose possible? Are they better or worse? Have they had any opportunity to be developed in cellular metabolism evolution? We have analyzed the Krebs cycle as a problem of chemical design to oxidize acetate yielding reduction equivalents to the respiratory chain to make ATP. Our analysis demonstrates that although there are several different chemical solutions to this problem, the design of this metabolic pathway as it occurs in living cells is the best chemical solution: It has the least possible number of steps and it also has the greatest ATP yielding. Study of the evolutionary possibilities of each one-taking the available material to build new pathways-demonstrates that the emergence of the Krebs cycle has been a typical case of opportunism in molecular evolution. Our analysis proves, therefore, that the role of opportunism in evolution has converted a problem of several possible chemical solutions into asingle-solution problem, with the actual Krebs cycle demonstrated to be the best possible chemical design. Our results also allow us to derive the rules under which metabolic pathways emerged during the origin of life.     

In the Beginning was a Mutualism - On the Origin of Translation

The origin of translation is critical for understanding the evolution of life, including the origins of life. The canonical genetic code is one of the most dominant aspects of life on this planet, while the origin of heredity is one of the key evolutionary transitions in living world. Why the translation apparatus evolved is one of the enduring mysteries of molecular biology. Assuming the hypothesis, that during the emergence of life evolution had to first involve autocatalytic systems which only subsequently acquired the capacity of genetic heredity, we propose and discuss possible mechanisms, basic aspects of the emergence and subsequent molecular evolution of translation and ribosomes, as well as enzymes as we know them today. It is possible, in this sense, to view the ribosome as a digital-to-analogue information converter. The proposed mechanism is based on the abilities and tendencies of short RNA and polypeptides to fold and to catalyse biochemical reactions. The proposed mechanism is in concordance with the hypothesis of a possible chemical co-evolution of RNA and proteins in the origin of the genetic code or even more generally at the early evolution of life on Earth. The possible abundance and availability of monomers at prebiotic conditions are considered in the mechanism. The hypothesis that early polypeptides were folding on the RNA scaffold is also considered and mutualism in molecular evolutionary development of RNA and peptides is favoured.