Neo-sex chromosomes and adaptive potential in tortricid pests (original) (raw)
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Since the beginning of early evolutionary studies, in fact since Darwin himself in his most famous work, “On the Origin of Species”, biologists have been trying to answer the question of how species arise and how they can achieve the necessary reproductive barriers that are required to allow mutation and selection to operate and differentiate a neo-species from the mother species. It is an accepted tenet of evolutionary biology that species evolve into new species which are direct descendants of the original species. The closer the relationship between species is, the higher the percentage of genetic homology is. Closely related species often show extremely high levels of genetic homology (at times as high as what is measured between local populations within the same species) while differing by balanced chromosomal rearrangements. The theory of chromosomal speciation has been often proposed as a mechanism for new species emergence and the subject of this thesis is a novel approach to analysis and theoretical modeling of how it operates, and how certain categories of mutations can reinforce its effects. Translocation and chromosomal rearrangements occur in all eukaryotes with measurable and relatively fixed probabilities. Chromosomal rearrangements are one-time single events that occur in one specific individual during gametogenesis and are a common type of mutation. They can affect the Darwinian fitness of the affected individual in a significant manner if the individual is mating with non-rearranged individuals as follows. In the case of translocated individuals, gametes show reduced fertility when crossed with nonrearranged individuals. This decrease in fertility is quantified as ½ for crosses between rearranged heterozygotes and Wild Type or rearranged homozygotes, and is due to unbalanced gametes resulting from incorrect segregation during meiosis. The decrease in fertility for crosses between rearranged heterozygotes is even higher (the resulting fertility of these crosses is 5/16, making the reduction in fertility 11/16) due to the possible combinations between gametes and the resulting imbalances. Within large interbreeding populations, due to the validity of the Hardy-Weinberg law, chromosomal rearrangements are lost from the gene pool in one or very few generations due to their negatively heterotic effect on the fitness of individuals carrying these mutations (negatively heterotic meaning it negatively affects the fitness of the heterozygote). Hardy-Weinberg equilibria are also the reason that, in large populations, evolution of new characteristics is very slow (becoming increasingly slower in proportion to the size of the population, reaching theoretical zero evolutionary speed for an infinitely large freely interbreeding population). Amongst all the possible chromosomal rearrangements, some are negatively heterotic while others are neutral or potentially positively heterotic (in a limited number of cases). This thesis focuses exclusively on the negatively heterotic rearrangements, since they are the only ones that can play a leading role in speciation, and will not go into details on the other rearrangements that are expected to be present in populations as polymorphisms that play no significant role in speciation. If we examine locally isolated populations, characterized by inbreeding and, potentially, founder effects, we observe how, through stochastic processes, fixation of negatively heterotic chromosomal rearrangements can occur. It is important to note how, in order for local fixation to occur, the size of the population must be very small (fixation relies on genetic drift and stochastic factors that become extremely improbable when the number of interbreeding members of the population increases). If a chromosomal rearrangement becomes fixed in a small population, this population will be characterized by having very similar genotypes which will be to some extent different from the average allelic frequencies within the founder population. This difference will be proportional to the variance in the original population. Amongst the negatively heterotic chromosomal rearrangements (nominally Tandem Fusions, Robertsonian Fusions, Reciprocal Translocations, X-autosome translocations, and, potentially, multiple inversions) we shall focus on Reciprocal Translocations, for which a theoretical model will be presented. Once a negatively heterotic chromosomal rearrangement has become fixed in a local population, if the new population has limited and sporadic interbreeding with the founder population, the members that breed with the founding population members will have a lower fitness than those who do not do so (this has been called the “reinforcement hypothesis”). As a result of this hypothesis, it has been proposed that, over a limited number of generations, strong mating barriers will evolve. A strong candidate for the reinforcement mechanism is represented by genes that control visible factors that differentiate the new population from the old, such as secondary sexual characters, which will be favorably selected if they distinguish the new population from the founding population and increase reproductive isolation. It is therefore proposed that the new population will rapidly evolve different secondary sexual characteristics as a result of this. By modification of the Hardy Weinberg equilibrium we can model the effects of hybridization and influx of Wild Type individuals into the new population. A modified version of the Hardy-Weinberg equilibrium is presented in this thesis which includes both the effect of the translocation and the effects of the translocation coupled with the emergence of reinforcement genes. Computer models based on these matings have been developed for this thesis and will be presented. The results of the simulations show how the founding population and the new population will either merge (in which case the new population will be absorbed into the founding population and the rearrangement will disappear within very few generations) or drift apart and become completely separate, non-interbreeding (or minimally interbreeding) populations. The model also shows how, when a population fixes a chromosomal translocation, it becomes very resistant to re-invasion by the WT karyotype, and shows the capability of resisting repeat influx of up to 4.0% of the entire population per generation by WT individuals without extinction. Higher percentages, however, rapidly result in the extinction of the NS karyotype (3/10 cases in up to 4.5% random influx per generation resulted in extinction before 10.000 generations and 10/10 when the random influx is raised to up to 5%). Once reinforcement genes appear, the model shows how they rapidly become established, albeit not fixated, in the population, and generate a much stronger barrier to introgression by WT individuals. The results of these simulations show how, once a rearranged population for a negatively heterotic chromosomal rearrangement has separated itself from the original population, such as described above, it only has two possible pathways available. The first is the pathway towards becoming a new species while the second is the one leading to extinction of the rearrangement and reabsorption into the original population. Given that translocations either disappear or give rise to new species, each translocation event that can be determined to exist between two related species must represent a single speciation event. As a side note, this mechanism points to how the evolutionary significance of Sexual reproduction lies in the fact that sexual populations are capable of speciation, while asexual ones are not. Sexual reproduction thus allows for adaptation through speciation and radiation. In a nutshell, speciation exists because of sexual reproduction and vice versa. Since sexually reproducing species can radiate by chromosomal speciation into different species, the existence of sexual reproduction provides a clear evolutionary advantage that offsets the associated costs. New species can adapt and respond quicker to evolutionary pressure due to the lower numbers that allow quicker fixation of beneficial mutations compared to large populations. They are, however, more prone to the risk of extinction (i.e. it’s an “all or nothing” game, where most newly formed chromosomal species will become rapidly extinct). Paradoxically, large interbreeding populations, which would be considered an evolutionary success, pay for this success by losing the capability to speciate. In large interbreeding populations, evolution only happens in response to large disruptions (epidemics, pandemics, food shortages leading to mass mortality, etc…) or over extremely long timeframes and numbers of generations. The proposed model can be further reinforced if the translocations occur in dominant males in small populations causing a higher chance of leading to speciation. The path to speciation begins with the appearance of a F1 generation of NS/WT hybrids followed, through inbreeding, by the appearance of homozygous NS/NS individuals in the F2 generation. Stochastic factors play a large role in this stage, with the general characteristic of the probability of speciation being very low in absolute terms. The study of statistics however teaches us that, in evolutionary terms, very low probability events happen all the time. Speciation events thus are an overall rare event which happens with variable frequencies based on the characteristics of the species of origin (habitat, mobility, reproductive mechanisms, etc…). Each of these characteristics can have major effect on the number of species that evolve within closely related taxa (thus providing an explanation for taxa where speciation appears to be a very common thing and taxa which appear unchanged and composed of a very limited number of species for millions or tens of millions of years).
Chromosomal evolution and speciation: a recombination-based approach
New Phytologist, 2003
Although karyotypic differences between species have long been recognized, the question of whether these mutations play a causal role in speciation remains unanswered. This is because most models of chromosomal speciation focus on underdominance, which presents a theoretical paradox in that the strength of an underdominant barrier is inversely proportional to its fixation probability. To counter this problem, a new model has been proposed that focuses on the modification of effective recombination rates, whereby rearrangements facilitate the build up of linkage disequilibrium in the presence of gene flow. This model is discussed, along with new supporting data from the Solanaceae.
Chromosomal rearrangements, genome reorganization, and speciation
Biology Bulletin, 2016
Historical analysis of studying chromosome changes in evolution allows better understanding of the current level of research in this area. Reorganizations of the genetic system due to chromosomal rearrangements have important evolutionary consequences and may lead to speciation. Despite the complexity of evaluating the primacy of chromosome changes in speciation events, such phenomena are possible and occur in nature, as recent studies have demonstrated.
Ancestral polymorphisms explain the role of chromosomal inversions in speciation
PLOS Genetics, 2018
Understanding the role of chromosomal inversions in speciation is a fundamental problem in evolutionary genetics. Here, we perform a comprehensive reconstruction of the evolutionary histories of the chromosomal inversions in Drosophila persimilis and D. pseudoobscura. We provide a solution to the puzzling origins of the selfish Sex-Ratio arrangement in D. persimilis and uncover surprising patterns of phylogenetic discordance on this chromosome. These patterns show that, contrary to widely held views, all fixed chromosomal inversions between D. persimilis and D. pseudoobscura were already present in their ancestral population long before the species split. Our results suggest that patterns of higher genomic divergence and an association of reproductive isolation genes with chromosomal inversions may be a direct consequence of incomplete lineage sorting of ancestral polymorphisms. These findings force a reconsideration of the role of chromosomal inversions in speciation, not as protectors of existing hybrid incompatibilities, but as fertile grounds for their formation.
Frontiers in Genetics, 2014
Many hypotheses have been put forth to explain the origin and spread of inversions, and their significance for speciation. Several recent genic models have proposed that inversions promote speciation with gene flow due to the adaptive significance of the genes contained within them and because of the effects inversions have on suppressing recombination. However, the consequences of inversions for the dynamics of genome wide divergence across the speciation continuum remain unclear, an issue we examine here. We review a framework for the genomics of speciation involving the congealing of the genome into alternate adaptive states representing species ("genome wide congealing"). We then place inversions in this context as examples of how genetic hitchhiking can potentially hasten genome wide congealing. Specifically, we use simulation models to (i) examine the conditions under which inversions may speed genome congealing and (ii) quantify predicted magnitudes of these effects. Effects of inversions on promoting speciation were most common and pronounced when inversions were initially fixed between populations before secondary contact and adaptation involved many genes with small fitness effects. Further work is required on the role of underdominance and epistasis between a few loci of major effect within inversions. The results highlight five important aspects of the roles of inversions in speciation: (i) the geographic context of the origins and spread of inversions, (ii) the conditions under which inversions can facilitate divergence, (iii) the magnitude of that facilitation, (iv) the extent to which the buildup of divergence is likely to be biased within vs. outside of inversions, and (v) the dynamics of the appearance and disappearance of exceptional divergence within inversions. We conclude by discussing the empirical challenges in showing that inversions play a central role in facilitating speciation with gene flow. tualized ideas, designed models, interpreted data, and wrote the paper. Samuel M. Flaxman programmed simulations.
The role of chromosomal inversions in speciation
The chromosomal inversions of D. persimilis and D. pseudoobscura have deeply influenced our understanding of the evolutionary forces that shape natural variation, speciation, and selfish chromosome dynamics. Here, we perform a comprehensive reconstruction of the evolutionary histories of the chromosomal inversions in these species. We provide a solution to the puzzling origins of the selfish Sex-Ratio chromosome in D. persimilis and show that this Sex-Ratio chromosome directly descends from an ancestrally-arranged chromosome. Our results further show that all fixed inversions between D. persimilis and D. pseudoobscura were segregating in the ancestral population long before speciation, and that the genes contributing to reproductive barriers between these species must have evolved within them afterwards. We propose a new model for the role of chromosomal inversions in speciation and suggest that higher levels of divergence and an association with hybrid incompatibilities are emergen...
Abstract Chromosomal rearrangements between sympatric species often contain multiple loci contributing to assortative mating, local adaptation, and hybrid sterility. When and how these associations arise during the process of speciation remains a subject of debate. Here, we address the relative roles of local adaptation and assortative mating on the dynamics of rearrangement evolution by studying how a rearrangement co-varies with sexual and ecological trait divergence within a species. Previously, a chromosomal rearrangement that suppresses recombination on the Z (sex) chromosome was identified in European corn borer moths (Ostrinia nubilalis). We further characterize this recombination suppressor and explore its association with variation in sex pheromone communication and seasonal ecological adaptation in pairs of populations that are divergent in one or both of these characteristics. Direct estimates of recombination suppression in pedigree mapping families indicated that more than 39% of the Z chromosome (encompassing up to ~10 megabases and ~ 300 genes) resides within a non-recombining unit, including pheromone olfactory receptor (OR) genes and a major quantitative trait locus (QTL) that contributes to ecotype differences (Pdd). Combining direct and indirect estimates of recombination suppression, we found that the rearrangement was occasionally present between sexually isolated strains (E versus Z) and between divergent ecotypes (univoltine versus bivoltine). However, it was only consistently present when populations differed in both sexual and ecological traits. Our results suggest that independent of the forces that drove the initial establishment of the rearrangement, a combination of sexual and ecological divergence is required for rearrangement spread during speciation.
CLINAL DISTRIBUTION OF A CHROMOSOMAL REARRANGEMENT: A PRECURSOR TO CHROMOSOMAL SPECIATION
Evolution, 2008
Geographically structured genetic variants provide an effective means to assess sources of natural selection and mechanisms of adaptation to local environments. Correlated selection pressures along environmental gradients favor subdivision of genomes through chromosomal rearrangement. This study examines populations of Drosophila americana to evaluate selection pressures affecting chromosomal forms distinguished by a centromeric fusion. Analyses of chromosomal polymorphism throughout the Mississippi River Valley in the central United States reveal the presence of a distinct latitudinal cline for the chromosomal rearrangement. The cline has a width of 623 km centered at 35.97°N and displays a characteristic sigmoid shape consistent with a balance between selection and dispersal. Extreme low temperature during January, an indicator of winter severity, was identified as the environmental variable that most accurately predicts arrangement frequency. An intriguing relationship identified between the chromosomal cline and operational sex ratio indicates that these alternative arrangements of the X chromosome may influence sex-specific survival. A hypothesis for the cline is presented wherein variation associated with the alternative chromosome forms influences distinct overwintering strategies. The resulting subdivision within the genome embodies a transitory stage of a speciation process in which locally adapted gene complexes provide a foundation for species formation.
Molecular Ecology, 2018
The gene arrangements of Drosophila have played a prominent role in the history of evolutionary biology from the original quantification of genetic diversity to current studies of the mechanisms for the origin and establishment of new inversion mutations within populations and their subsequent fixation between species supporting reproductive barriers. This review examines the genetic causes and consequences of inversions as recombination suppressors and the role that recombination suppression plays in establishing inversions in populations as they are involved in adaptation within heterogeneous environments. This often results in the formation of clines of gene arrangement frequencies among populations. Recombination suppression leads to the differentiation of the gene arrangements which may accelerate the accumulation of fixed genetic differences among populations. If these fixed mutations cause incompatibilities, then inversions pose important reproductive barriers between species. This review uses the evolution of inversions in Drosophila pseudoobscura and D. persimilis as a case study for how inversions originate, establish, and contribute to the evolution of reproductive isolation.