Evolution is frequently concentrated in bursts of rapid morphological change and speciation followed by long-term stasis. We propose that this pattern of punctuated equilibria results from an ...evolutionary tug-of-war between host genomes and transposable elements (TEs) mediated through the epigenome. According to this hypothesis, epigenetic regulatory mechanisms (RNA interference, DNA methylation and histone modifications) maintain stasis by suppressing TE mobilization. However, physiological stress, induced by climate change or invasion of new habitats, disrupts epigenetic regulation and unleashes TEs. With their capacity to drive non-adaptive host evolution, mobilized TEs can restructure the genome and displace populations from adaptive peaks, thus providing an escape from stasis and generating genetic innovations required for rapid diversification. This "epi-transposon hypothesis" can not only explain macroevolutionary tempo and mode, but may also resolve other long-standing controversies, such as Wright's shifting balance theory, Mayr's peripheral isolates model, and McClintock's view of genome restructuring as an adaptive response to challenge.
Abstract
Long-branch attraction is a systematic artifact that results in erroneous groupings of fast-evolving taxa. The combination of short, deep internodes in tandem with long-branch attraction ...artifacts has produced empirically intractable parts of the Tree of Life. One such group is the arthropod subphylum Chelicerata, whose backbone phylogeny has remained unstable despite improvements in phylogenetic methods and genome-scale data sets. Pseudoscorpion placement is particularly variable across data sets and analytical frameworks, with this group either clustering with other long-branch orders or with Arachnopulmonata (scorpions and tetrapulmonates). To surmount long-branch attraction, we investigated the effect of taxonomic sampling via sequential deletion of basally branching pseudoscorpion superfamilies, as well as varying gene occupancy thresholds in supermatrices. We show that concatenated supermatrices and coalescent-based summary species tree approaches support a sister group relationship of pseudoscorpions and scorpions, when more of the basally branching taxa are sampled. Matrix completeness had demonstrably less influence on tree topology. As an external arbiter of phylogenetic placement, we leveraged the recent discovery of an ancient genome duplication in the common ancestor of Arachnopulmonata as a litmus test for competing hypotheses of pseudoscorpion relationships. We generated a high-quality developmental transcriptome and the first genome for pseudoscorpions to assess the incidence of arachnopulmonate-specific duplications (e.g., homeobox genes and miRNAs). Our results support the inclusion of pseudoscorpions in Arachnopulmonata (new definition), as the sister group of scorpions. Panscorpiones (new name) is proposed for the clade uniting Scorpiones and Pseudoscorpiones.
Although it is generally accepted that females can gain material benefits by mating with more than one male, the proposal that polyandry provides genetic benefits remains controversial, largely ...because direct experimental support is lacking. Here, we report the results of a study testing for genetic benefits to polyandry in the pseudoscorpion Cordylochernes scorpioides. In an experiment that controlled for male mating experience and the number of spermatophores accepted by a female, twice-mated females received either one sperm-packet from each of two different males (the "DM" treatment) or two sperm-packets from a single male (the same male or "SM" treatment). Over their lifetime, DM females gave birth to 32% more offspring than did SM females, primarily because of a significantly reduced rate of spontaneous abortion. This result could not be attributed to male infertility nor to lack of sexual receptivity in males paired with previous mates. Spermatophore and sperm numbers did not differ between males presented with a previous mate and males paired with a new female. Because SM and DM females received the same quantity of ejaculate, it was possible to eliminate material benefits as a contributor to the enhanced reproductive success of DM females. The reduction in embryo failure rate achieved by DM females is most consistent with the genetic incompatibility avoidance hypothesis, i.e., that polyandry enables females to exploit postcopulatory mechanisms for reducing the risk and/or cost of fertilization by genetically incompatible sperm. This study, which rigorously controlled for material benefits and excluded inbreeding effects, demonstrates that polyandry provides genetic benefits that significantly enhance female lifetime reproductive success.
Darwin's recognition that male–male competition and female choice could favor the evolution of exaggerated male traits detrimental to survival set the stage for more than a century of theoretical and ...empirical work on sexual selection. While this Darwinian paradigm represents one of the most profound insights in biology, its preoccupation with sexual selection as a directional evolutionary force acting on males has diverted attention away from the selective processes acting on females. Our understanding of female reproduction has been further confounded by discreet female mating tactics that have perpetuated the illusion of the monogamous female and masked the potential for conflict between the sexes. With advances in molecular techniques leading to the discovery that polyandry is a pervasive mating strategy, recognition of these shortcomings has brought the study of sexual selection to its current state of flux. In this paper, we suggest that progress in two key areas is critical to formulation of a more inclusive, sexual selection paradigm that adequately incorporates selection from the female perspective. First, we need to develop a better understanding of male × female and maternal × paternal genome interactions and the role that polyandry plays in providing females with non‐additive genetic benefits such as incompatibility avoidance. Consideration of these interaction effects influencing natural selection on females is important because they can complicate and even undermine directional sexual selection on males. Secondly, because antagonistic coevolution maintains a balance between opposing sides that obscures the conflict itself, many more experimental evolution studies and interventionist investigations (e.g. gene knockouts) are needed to tease apart male manipulative adaptations and female counter‐adaptations. It seems evident that the divisiveness and controversy that has plagued sexual selection theory since Darwin first proposed the idea has often stalled progress in this important field of evolutionary biology. What is now needed is a more pluralistic and integrative approach that considers natural as well as sexual selection acting on females, incorporates multiple sexual selection mechanisms, and exploits advances in physiology and molecular biology to understand the mechanisms through which males and females achieve reproductive success.
Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural ...world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.
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Dostopno za:
DOBA, IJS, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Fundamental to the recently-proposed hypothesis that females mate with more than one male as a hedge against genetic incompatibility is the premise that mechanisms are available to polyandrous ...females which enable them to safeguard their reproductive investment against the threat of incompatibility between maternal and paternal genomes. Accumulation of sperm from several males shifts the arena for sexual selection from the external environment to the female reproductive tract where, we suggest, interactions at the molecular and cellular levels provide females with direct mechanisms for assessing genetic compatibility. We present examples from the literature to illustrate how sperm competition and female choice of sperm can enable polyandrous females to minimize the risk of fertilization by genetically-incompatible sperm. Polyandry and multiple paternity also create the opportunity to reduce the cost of genetic incompatibility by reallocation of maternal resources from defective to viable offspring. This is likely to be a critically important post-copulatory mechanism for viviparous females whose intimate immunological relationship with developing embryos makes them particularly vulnerable to genetic incompatibility arising from intragenomic conflict and other processes acting at the suborganismal level.
Behavioural ecology is currently undergoing a paradigm shift, with the traditional concepts of the choosy, monogamous female and the coadapted gene complex increasingly giving way to the realization ...that sexual reproduction engenders conflicts, promotes polyandry, and thereby provides females with a cryptic arsenal of postcopulatory processes with which to safeguard their investment in large, costly eggs. As research focuses on reproduction from the female perspective, evidence is emerging that polyandry can provide genetic benefits that enhance female reproductive success. In this review, we propose that reproductive mode is a critically important factor influencing the type of genetic benefits that females gain by mating with more than one male. Among the hypotheses that propose genetic benefits to polyandry, there is a distinction between those that posit benefits from intrinsic (additive) effects of paternal genes in offspring, and those that propose a benefit resulting from defence against incompatibility. Polyandry to acquire superior paternal genes and polyandry as a defence against incompatibility are not mutually exclusive hypotheses. However, evidence from reproductive physiology, immunology and evolutionary conflict theory suggest that development of the embryo within the female makes polyandry for incompatibility avoidance far more important for viviparous females than for females that lay eggs.
Female choice for traits signaling male genetic quality is expected to erode heritable variation in fitness, undermining the benefits of choice. Known as the lek paradox, this contradiction has ...motivated extensive population genetic theory, yet remains unresolved. Recent modeling by Bonduriansky and Day concludes that costly female preference is best maintained when male condition is determined by environmentally induced factors transmitted across single generations. Here, we reformulate their model in explicitly epigenetic terms, and review evidence that environmentally induced paternal effects are mediated through epigenetic changes in sperm. Noncoding RNA expression, DNA methylation and histone modifications are highly sensitive to diet, stress, toxicants and stochastic events. Epigenetic variation renews each generation and cannot be exhausted by selection. By choosing well‐endowed males that produce gametes in epigenetically good states, females can increase their fitness directly through increased fertilization success or indirectly through epigenetic effects on the fitness of offspring and potentially subsequent generations.
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Variation in diet, stress, and exercise affects male sexually selected trait expression and sperm epigenetic profiles that modulate offspring development, growth, and reproduction. Transmission of male condition via sperm‐borne epigenetic states provides a parsimonious explanation for the maintenance of adaptive female choice and heritable variation in male attractiveness and quality.
Although climate change models predict relatively modest increases in temperature in the tropics by the end of the century, recent analyses identify tropical ectotherms as the organisms most at risk ...from climate warming. Because metabolic rate in ectotherms increases exponentially with temperature, even a small rise in temperature poses a physiological threat to tropical ectotherms inhabiting an already hot environment. If correct, the metabolic theory of climate warming has profound implications for global biodiversity, since tropical insects and arachnids constitute the vast majority of animal species. Predicting how climate change will translate into fitness consequences for tropical arthropods requires an understanding of the effects of temperature increase on the entire life history of the species. Here, in a comprehensive case study of the fitness consequences of the projected temperature increase for the tropics, we conducted a split‐brood experiment on the neotropical pseudoscorpion, Cordylochernes scorpioides, in which 792 offspring from 33 females were randomly assigned at birth to control‐ and high‐temperature treatments for rearing through the adult stage. The diurnally varying, control treatment temperature was determined from long‐term, average daily temperature minima and maxima in the pseudoscorpion's native habitat. In the high temperature treatment, increasing temperature by the 3.5 °C predicted for the tropics significantly reduced survival and accelerated development at the cost of reduced adult size and a dramatic decrease in level of sexual dimorphism. The most striking effects, however, involved reproductive traits. Reared at high temperature, males produced 45% as many sperm as control males, and females failed to reproduce. Sequencing of the mitochondrial ND2 gene revealed two highly divergent haplogroups that differed substantially in developmental rate and survivorship but not in reproductive response to high temperature. Our findings suggest that reproduction may be the Achilles’ heel of tropical ectotherms, as climate warming subjects them to an increasingly adverse thermal environment.
Why do females across a wide range of taxa mate with more than one male? We suggest that a better understanding of polyandry may be gained by considering the implications of intragenomic conflict for ...female reproductive success. Here, we revisit the literature on cellular endosymbionts, transposable elements, segregation distorters, maternal-effect lethals and genomically imprinted genes to show that each of these selfish genetic elements can modify maternal and paternal haplotypes in ways that render them incompatible within the developing embryo. We propose that the cumulative threat to female reproductive success of genetic incompatibility arising from intragenomic conflict may be an important force driving the evolution of polyandry. By mating with more than one male, females can potentially exploit post-copulatory mechanisms for minimizing the risk and/or cost of fertilization by genetically incompatible sperm. This hypothesis differs fundamentally from other genetic benefit models of polyandry in that the fitness consequences of intragenomic conflict depend on an interaction between parental genomes and are thus non-additive. Reciprocal evolutionary change between selfish genetic elements and their suppressors, combined with the capacity of these elements for horizontal transfer between species, is likely to ensure the persistence of genetic incompatibility as a threat to female reproductive success.
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