Most organisms reproduce through outcrossing, even though it comes with significant costs. The Red Queen hypothesis proposes that selection from coevolving pathogens facilitates the persistence of outcrossing in spite of these costs. We utilized experimental coevolution to test the Red Queen hypothesis, and found that coevolution with a bacterial pathogen (Serratia marcescens) resulted in significantly more outcrossing in mixed mating experimental populations of the nematode Caenorhabditis elegans. Furthermore, we found that coevolution with the pathogen rapidly drove obligately selfing populations to extinction, while outcrossing populations persisted through reciprocal coevolution. Thus, consistent with the Red Queen hypothesis, coevolving pathogens can select for biparental sex.
The tendency of organisms to reproduce by cross-fertilization despite numerous disadvantages relative to self-fertilization is one of the oldest puzzles in evolutionary biology. For many species, the primary obstacle to the evolution of outcrossing is the cost of producing of males1, individuals that do not directly contribute offspring and thus diminish the long-term reproductive output of a lineage. Self-fertilizing organisms do not incur the cost of males and therefore should possess at least a two-fold numerical advantage over most outcrossing organisms2. Two competing explanations for the widespread prevalence of outcrossing in nature despite this inherent disadvantage are the avoidance of inbreeding depression generated by selfing3–5 and the ability of outcrossing populations to more rapidly adapt to environmental change1,6,7. Here we show that outcrossing is favored in populations of C. elegans subject to experimental evolution both under conditions of increased mutation rate and during adaptation to a novel environment. In general, fitness increased with increasing rates of outcrossing. Thus, each of the standard explanations for the maintenance of outcrossing are correct, and it is likely that outcrossing is the predominate mode of reproduction in most species because it is favored under ecological conditions that are ubiquitous in natural environments.
Caenorhabditis elegans is an androdioecious nematode with both hermaphrodites and males. Although males can potentially play an important role in avoiding inbreeding and facilitating adaptation, their existence is evolutionarily problematic because they do not directly generate offspring in the way that hermaphrodites do. This review explores how genetic, population genomic, and experimental evolution approaches are being used to address the role of males and outcrossing within C. elegans. Although theory suggests that inbreeding depression and male mating ability should be the primary determinants of male frequency, this has yet to be convincingly confirmed experimentally. Genomic analysis of natural populations finds that outcrossing occurs at low, but not negligible levels, and that observed patterns of linkage disequilibrium consistent with strong selfing may instead be generated by natural selection against outcrossed progeny. Recent experimental evolution studies suggest that males can be maintained at fairly high levels if populations are initiated with sufficient genetic variation and/or subjected to strong natural selection via a change in the environment. For example, as reported here, populations adapting to novel laboratory rearing and temperature regimes maintain males at frequencies from 5% to 40%. Laboratory and field results still await full reconciliation, which may be facilitated by identifying the loci underlying among-strain differences in mating system dynamics.
Sexual reproduction shuffles genetic variation, potentially enhancing the evolutionary response to environmental change. Many asexual organisms utilize facultative sexual reproduction as a means to escape the trap of low genetic diversity under stress. Self-fertilizing organisms are subject to similar genetic limitations: the consistent loss of genetic diversity within lineages restricts the production of variation through recombination. Selfing organisms may therefore benefit from a similar shift in mating strategy during periods of stress. We determined the effects of environmental stress via starvation and exposure to the stress-resistant dauer stage on mating system dynamics of Caenorhabditis elegans, which reproduces predominantly through self-fertilization but is capable of outcrossing in the presence of males. Starvation elevated male frequencies in a strain-specific manner through differential male survival during dauer exposure and increased outcrossing rates after dauer exposure. In the most responsive strain, the mating system changed from predominantly selfing to almost exclusively outcrossing. Like facultative sex in asexual organisms, facultative outcrossing in C. elegans may periodically facilitate adaptation under stress. Such a shift in reproductive strategy should have a major impact on evolutionary change within these populations and may be a previously unrecognized feature of other highly selfing organisms.
Males of Caenorhabditis elegans provide a crucial practical tool in the laboratory, but, as the rarer and more finicky sex, have not enjoyed the same depth of research attention as hermaphrodites. Males, however, have attracted the attention of evolutionary biologists who are exploiting the C. elegans system to test longstanding hypotheses about sexual selection, sexual conflict, transitions in reproductive mode, and genome evolution, as well as to make new discoveries about Caenorhabditis organismal biology. Here, we review the evolutionary concepts and data informed by study of males of C. elegans and other Caenorhabditis. We give special attention to the important role of sperm cells as a mediator of inter-male competition and male–female conflict that has led to drastic trait divergence across species, despite exceptional phenotypic conservation in many other morphological features. We discuss the evolutionary forces important in the origins of reproductive mode transitions from males being common (gonochorism: females and males) to rare (androdioecy: hermaphrodites and males) and the factors that modulate male frequency in extant androdioecious populations, including the potential influence of selective interference, host–pathogen coevolution, and mutation accumulation. Further, we summarize the consequences of males being common vs rare for adaptation and for trait divergence, trait degradation, and trait dimorphism between the sexes, as well as for molecular evolution of the genome, at both micro-evolutionary and macro-evolutionary timescales. We conclude that C. elegans male biology remains underexploited and that future studies leveraging its extensive experimental resources are poised to discover novel biology and to inform profound questions about animal function and evolution.
Many mutations that dramatically extend life span in model organisms come with substantial fitness costs. Although these genetic manipulations provide valuable insight into molecular modulators of life span, it is currently unclear whether life-span extension is unavoidably linked to fitness costs. To examine this relationship, we evolved a genetically heterogeneous population of Caenorhabditis elegans for 47 generations, selecting for early fecundity. We asked whether an increase in early fecundity would necessitate a decrease in longevity or late fecundity (antagonistic pleiotropy). Caenorhabditis elegans experimentally evolved for increased early reproduction and decreased late reproduction but suffered no total fitness or life-span costs. Given that antagonistic pleiotropy among these traits has been previously demonstrated in some cases, we conclude that the genetic constraint is not absolute, that is, it is possible to uncouple longevity from early fecundity using genetic variation segregating within and among natural populations.
Sexual reproduction is widely regarded as one of the major unexplained phenomena in biology. Nonetheless, while a general answer may remain elusive, considerable progress has been made in the last few decades. Here we fist review the genesis of, and support for, the major ecological hypotheses for biparental sexual reproduction. We then focus on the idea that host-parasite coevolution can favor cross fertilization over uniparental forms of reproduction, as this hypothesis currently has the most support from natural populations. We also review the results from experimental evolution studies, which tend to show that exposure to novel environments can select for higher levels of sexual reproduction, but that sex decreases in frequency after populations become adapted to the previously novel conditions. In contrast, experimental coevolution studies suggest that host-parasite interactions can lead to the long-term persistence of sex. Taken together, the evidence from natural populations and from laboratory experiments point to antagonistic coevolution as a potent and possibly ubiquitous force of selection favoring cross-fertilization and recombination.
Microorganisms play a significant role in the evolution and functioning of the eukaryotes with which they interact. Much of our understanding of beneficial host–microbe interactions stems from studying already established associations; we often infer the genotypic and environmental conditions that led to the existing host–microbe relationships. However, several outstanding questions remain, including understanding how host and microbial (internal) traits, and ecological and evolutionary (external) processes, influence the origin of beneficial host–microbe associations. Experimental evolution has helped address a range of evolutionary and ecological questions across different model systems; however, it has been greatly underutilized as a tool to study beneficial host–microbe associations. In this review, we suggest ways in which experimental evolution can further our understanding of the proximate and ultimate mechanisms shaping mutualistic interactions between eukaryotic hosts and microbes. By tracking beneficial interactions under defined conditions or evolving novel associations among hosts and microbes with little prior evolutionary interaction, we can link specific genotypes to phenotypes that can be directly measured. Moreover, this approach will help address existing puzzles in beneficial symbiosis research: how symbioses evolve, how symbioses are maintained, and how both host and microbe influence their partner’s evolutionary trajectories. By bridging theoretical predictions and empirical tests, experimental evolution provides us with another approach to test hypotheses regarding the evolution of beneficial host–microbe associations.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.