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Data from: Haploids adapt faster than diploids across a range of environments
Gerstein, Aleeza C; Cleathero, Lesley A; Mandegar, Mohammad A; Otto, Sarah P. — 2010-12-07 Despite a great deal of theoretical attention, we have limited empirical data about how ploidy influences the rate of adaptation. We evolved isogenic haploid and diploid populations of Saccharomyces cerevisiae for 200 generations in seven different environments. We measured the competitive fitness of all ancestral and evolved lines against a common competitor and find that in all seven environments haploid lines adapted faster than diploids, significantly so in three environments. We apply theory that relates the rates of adaptation and measured effective population sizes to the properties of beneficial mutations. We obtained rough estimates of the average selection coefficients in haploids between 2-10% for these first selected mutations. Results were consistent with semi-dominant to dominant mutations in four environments and recessive to additive mutations in two other environments. These results are consistent with theory that predicts haploids should evolve faster than diploids at large population sizes.
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Data from: Evolutionarily stable sex ratios and mutation load
Hough, Josh; Immler, Simone; Barrett, Spencer C. H.; Otto, Sarah P. — 2013-01-16 Frequency-dependent selection should drive dioecious populations toward a 1:1 sex ratio, but biased sex ratios are widespread, especially among plants with sex chromosomes. Here, we develop population genetic models to investigate the relationships between evolutionarily stable sex ratios, haploid selection, and deleterious mutation load. We confirm that when haploid selection acts only on the relative fitness of X and Y-bearing pollen and the sex ratio is controlled by the maternal genotype, seed sex ratios evolve toward 1:1. When we also consider haploid selection acting on deleterious mutations, however, we find that biased sex ratios can be stably maintained, reflecting a balance between the advantages of purging deleterious mutations via haploid selection, and the disadvantages of haploid selection on the sex ratio. Our results provide a plausible evolutionary explanation for biased sex ratios in dioecious plants, given the extensive gene expression that occurs across plant genomes at the haploid stage.
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On the evolutionary epidemiology of SARS-CoV-2
Day, Troy; Gandon, Sylvain; Lion, Sébastien; Otto, Sarah P. — 2020-06-24 <p><span><span style="font-style:normal;"><span><span style="font-weight:normal;"><span style="letter-spacing:normal;"><span><span><span style="white-space:normal;"><span><span><span>There is no doubt that the novel coronavirus SARS-CoV-2 that causes COVID-19 is mutating and thus has the potential to adapt during the current pandemic. Whether this evolution will lead to changes in the transmission, the duration, or the severity of the disease is not clear. This has led to considerable scientific and media debate, from raising alarms about evolutionary change to dismissing it. Here we review what little is currently known about the evolution of SARS-CoV-2 and extend existing evolutionary theory to consider how this disease might evolve during the COVID-19 pandemic. While there is currently no definitive evidence that SARS-CoV-2 is undergoing further adaptation, continued, evidence-based, analysis of evolutionary change is important so that public health measures can be adjusted in response to substantive changes in the infectivity or severity of COVID-19.</span></span></span></span></span></span></span></span></span></span></span></p>
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Data from: Evolution of haploid selection in predominantly diploid organisms
Otto, Sarah P.; Scott, Michael F.; Immler, Simone — 2016-12-01 Diploid organisms manipulate the extent to which their haploid gametes experience selection. Animals typically produce sperm with a diploid complement of most proteins and RNA, limiting selection on the haploid genotype. Plants, however, exhibit extensive expression in pollen, with actively transcribed haploid genomes. Here we analyze models that track the evolution of genes that modify the strength of haploid selection to predict when evolution intensifies and when it dampens the “selective arena” within which male gametes compete for fertilization. Considering deleterious mutations, evolution leads diploid mothers to strengthen selection among haploid sperm/pollen, because this reduces the mutation load inherited by their diploid offspring. If, however, selection acts in opposite directions in haploids and diploids (“ploidally antagonistic selection”), mothers evolve to reduce haploid selection to avoid selectively amplifying alleles harmful to their offspring. Consequently, with maternal control, selection in the haploid phase either is maximized or reaches an intermediate state, depending on the deleterious mutation rate relative to the extent of ploidally antagonistic selection. By contrast, evolution generally leads diploid fathers to mask mutations in their gametes to the maximum extent possible, whenever masking (e.g., through transcript sharing) increases the average fitness of a father’s gametes. We discuss the implications of this maternal–paternal conflict over the extent of haploid selection and describe empirical studies needed to refine our understanding of haploid selection among seemingly diploid organisms.
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Data from: Phylogenetic evidence for cladogenetic polyploidization in land plants
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Zhan, Shing Hei; Drori, Michal; Goldberg, Emma E.; Otto, Sarah P.; Mayrose, Itay — 2017-07-15 Premise of the study: Polyploidization is a common and recurring phenomenon in plants and is often thought to be a mechanism of "instant speciation." Whether polyploidization is associated with the formation of new species ("cladogenesis") or simply occurs over time within a lineage ("anagenesis") has never, however, been assessed systematically. Methods: Here, we tested this hypothesis using phylogenetic and karyotypic information from 235 plant genera (mostly angiosperms). We first constructed a large database of combined sequence and chromosome number data sets using an automated procedure. We then applied likelihood models (ClaSSE) that estimate the degree of synchronization between polyploidization and speciation events in maximum likelihood and Bayesian frameworks. Key results: Our maximum likelihood analysis indicated that 35 genera supported a model that includes cladogenetic transitions over a model with only anagenetic transitions, whereas three genera supported a model that incorporates anagenetic transitions over one with only cladogenetic transitions. Furthermore, the Bayesian analysis supported a preponderance of cladogenetic change in four genera but did not support a preponderance of anagenetic change in any genus. Conclusions: Overall, these phylogenetic analyses provide the first broad confirmation that polyploidization is temporally associated with speciation events, suggesting that it is indeed a major speciation mechanism in plants, at least in some genera.
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Data from: Costs of reproduction explain the correlated evolution of semelparity and egg size: theory and a test with salmon
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Braun, Douglas C.; Kindsvater, Holly K.; Otto, Sarah P.; Reynolds, John D. — 2017-03-21 Species’ life history traits, including maturation age, number of reproductive bouts, offspring size and number, reflect adaptations to diverse biotic and abiotic selection pressures. A striking example of divergent life histories is the evolution of either iteroparity (breeding multiple times) or semelparity (breed once and die). We analysed published data on salmonid fishes and found that semelparous species produce larger eggs, that egg size and number increase with salmonid body size among populations and species and that migratory behaviour and parity interact. We developed three hypotheses that might explain the patterns in our data and evaluated them in a stage-structured modelling framework accounting for different growth and survival scenarios. Our models predict the observation of small eggs in iteroparous species when egg size is costly to maternal survival or egg number is constrained. By exploring trait co-variation in salmonids, we generate new hypotheses for the evolution of trade-offs among life history traits.
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Data from: Adaptation to elevated CO2 in different biodiversity contexts
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Kleynhans, Elizabeth J.; Otto, Sarah P.; Reich, Peter B.; Vellend, Mark — 2017-06-03 In the absence of migration, species persistence depends on adaption to a changing environment, but whether and how adaptation to global change is altered by community diversity is not understood. Community diversity may prevent, enhance or alter how species adapt to changing conditions by influencing population sizes, genetic diversity and/or the fitness landscape experienced by focal species. We tested the impact of community diversity on adaptation by performing a reciprocal transplant experiment on grasses that evolved for 14 years under ambient and elevated CO2, in communities of low or high species-richness. Using biomass as a fitness proxy, we find evidence for local adaptation to elevated CO2, but only for plants assayed in a community of similar diversity to the one experienced during the period of selection. Our results indicate that the biological community shapes the very nature of the fitness landscape within which species evolve in response to elevated CO2.
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Data from: Establishment and maintenance of adaptive genetic divergence under migration, selection, and drift
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Yeaman, Sam; Otto, Sarah P. — 2011-02-24 There is a long tradition in population genetics of exploring the maintenance of variation under migration-selection balance using deterministic models that assume infinite population size. With finite population size, stochastic dynamics can greatly reduce the potential for the maintenance of polymorphism, but this has yet to be explored in detail. Here, classical two-patch models are extended to predict: i) the probability of a locally beneficial mutation rising in frequency in the patch where it is favored, and ii) the critical threshold migration rate above which the maintenance of polymorphism is much less likely. Individual-based simulations show that these approximations provide accurate predictions across a wide range of parameter space.
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Data from: Recently-formed polyploid plants diversify at lower rates
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Mayrose, Itay; Zhan, Shing H.; Rothfels, Carl J.; Magnuson-Ford, Karen; Barker, Michael S.; Rieseberg, Loren H.; Otto, Sarah P. — 2011-08-19 Polyploidy, the doubling of genomic content, is a widespread feature, especially among plants, yet its macro-evolutionary impacts are contentious. Traditionally, polyploidy has been considered an evolutionary dead-end, whereas recent genomic studies suggest that polyploidy has been a key driver of macro-evolutionary success. Here we examine the consequences of polyploidy on the time scale of genera across a diverse set of vascular plants, encompassing hundreds of inferred polyploidization events. Likelihood-based analyses indicate that polyploids generally exhibit lower speciation rates and higher extinction rates than diploids, providing the first quantitative corroboration of the dead-end hypothesis. The increased speciation rates of diploids can, in part, be ascribed to their capacity to speciate via polyploidy. Only particularly “fit” lineages of polyploids may persist to enjoy longer term evolutionary success.
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Data from: Liking the good guys: amplifying local adaptation via the evolution of condition-dependent mate choice
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Veen, Thor; Otto, Sarah P. — 2015-07-20 Local adaptation can be strengthened through a diversity of mechanisms that reduce gene flow between contrasting environments. Recent work revealed that mate choice could enhance local adaptation when females preferentially mate with locally adapted males and that such female preferences readily evolve, but the opposing effects of recombination, migration, and costs of female preferences remain relatively unexplored. To investigate these effects, we develop a two-patch model with two genes, one influencing an ecological trait and one influencing female preferences, where both male signals and female preferences are allowed to depend on the match between an individual's ecological trait and the local environment (condition). Because trait variation is limited when migration is rare and the benefits of preferential mating are short-lived when migration is frequent, we find that female preferences for males in high condition spread most rapidly with intermediate levels of migration. Surprisingly, we find that preferences for locally adapted males spread fastest with higher recombination rates, which contrasts with earlier studies. This is because a stronger preference allele for locally adapted males can only get uncoupled from maladapted ecological alleles following migration through recombination. The effects of migration and recombination depend strongly on the condition of the males being chosen by females, but only weakly on the condition of the females doing the choosing, except when it comes to the costs of preference. While costs always impede the spread of female preferences for locally adapted males, the impact is substantially lessened if costs are borne primarily by females in poor condition. The abundance of empirical examples of condition-dependent mate choice combined with our theoretical results suggests that the evolution of mate choice could commonly facilitate local adaptation in nature.
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Data from: The red queen coupled with directional selection favors the evolution of sex
Hodgson, Emma E.; Otto, Sarah P. — 2012-01-30 Why sexual reproduction has evolved to be such a widespread mode of reproduction remains a major question in evolutionary biology. While previous studies have shown that increased sex and recombination can evolve in the presence of host-parasite interactions (the “Red Queen hypothesis” for sex), many of these studies have assumed that multiple loci mediate infection versus resistance. Data suggest, however, that a major locus is typically involved in antigen presentation and recognition. Here, we explore a model where only one locus mediates host-parasite interactions, but a second locus is subject to directional selection. Even though the effects of these genes on fitness are independent, we show that increased rates of sex and recombination are favored at a modifier gene that alters the rate of genetic mixing. This result occurs because of selective interference that occurs in finite populations (the “Hill-Robertson effect”), which also favors sex. These results suggest that the Red Queen hypothesis may help to explain the evolution of sex by contributing a form of persistent selection, which interferes with directional selection at other loci and thereby favors sex and recombination.

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(Author: Otto, Sarah P.)

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