{"title":"A gene-based model of fitness and its implications for genetic variation","authors":"Parul Johri, Brian Charlesworth","doi":"10.1101/2024.09.12.612686","DOIUrl":"https://doi.org/10.1101/2024.09.12.612686","url":null,"abstract":"A widely used model of the effects of mutations on fitness (the ″sites″ model) assumes that heterozygous recessive or partially recessive deleterious mutations at different sites in a gene complement each other, similarly to mutations in different genes. However, the general lack of complementation between major effect allelic mutations suggests an alternative possibility, the ″gene″ model. This assumes that a pair of heterozygous deleterious mutations in <em>trans</em> behave effectively as homozygotes, so that the fitnesses of <em>trans</em> heterozygotes are lower than those of <em>cis</em> heterozygotes. We examine the properties of the two different models, using both analytical and simulation methods. We show that the gene model results in a slightly lower mutational load, but a much smaller inbreeding load, than the sites model, implying that standard predictions of mutational contributions to inbreeding depression may be overestimates. The gene model also predicts positive linkage disequilibrium (LD) between derived variants within the coding sequence under conditions when the sites model predicts zero or slightly negative LD. We also show that focussing on rare variants when examining patterns of LD, especially with Lewontin′s D′ measure, is likely to produce misleading results with respect to inferences concerning the causes of the sign of LD. Synergistic epistasis between pairs of mutations was also modeled; it is less likely to produce negative LD under the gene model than the sites model. The theoretical results are discussed in relation to data on inbreeding load in <em>Drosophila melanogaster</em> and patterns of LD in natural populations of several species.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"8 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264568","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Isolating selective from non-selective forces using site frequency ratios","authors":"Jody Hey, Vitor Pavinato","doi":"10.1101/2024.09.13.612810","DOIUrl":"https://doi.org/10.1101/2024.09.13.612810","url":null,"abstract":"A new method is introduced for estimating the distribution of mutation fitness effects using site frequency spectra. Unlike previous methods, which make assumptions about non-selective factors, or that try to incorporate such factors into the underlying model, this new method mostly avoids non-selective effects by working with the ratios of counts of selected sites to neutral sites. An expression for the likelihood of a set of selected/neutral ratios is found by treating the ratio of two Poisson random variables as the ratio of two gaussian random variables. This approach also avoids the need to estimate the relative mutation rates of selected and neutral sites. Simulations over a wide range of demographic models, with linked selection effects show that the new SF-Ratios method performs well for statistical tests of selection, and it performs well for estimating the distribution of selection effects. Applications to two populations of Drosophila melanogaster reveal clear but very weak selection on synonymous sites. For nonsynonymous sites, selection was estimated to be far weaker than previous estimates for Drosophila populations.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"195 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264566","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Alexandre Rego, Julian Baur, Camille Girard-Tercieux, Maria de la Paz Celorio-Mancera, Rike Stelkens, David Berger
{"title":"Strong Selection, but low repeatability: Temperature-specific effects on genomic predictions of adaptation","authors":"Alexandre Rego, Julian Baur, Camille Girard-Tercieux, Maria de la Paz Celorio-Mancera, Rike Stelkens, David Berger","doi":"10.1101/2024.09.12.612579","DOIUrl":"https://doi.org/10.1101/2024.09.12.612579","url":null,"abstract":"Evolution should be more predictable when natural selection is strong and favors the same outcome. Climate warming is increasing temperatures beyond the optima of many ectotherms, which, due to the inherent non-linear relationship between temperature and the rate of cellular processes, is predicted to impose stronger selection compared to corresponding shifts toward cold temperatures. This suggests that adaptation to climate warming should be relatively predictable. Here, we tested this hypothesis from the level of single-nucleotide polymorphisms to life-history traits, by conducting an evolve-and-resequence experiment on three genetic backgrounds of the seed beetle, Callosobruchus maculatus. Indeed, phenotypic evolution was faster and more repeatable at hot, relative to cold, temperature. However, at the genomic level, adaptation to heat was less repeatable than to cold, especially when comparing responses between backgrounds. As a result, genomic predictions of phenotypic (mal)adaptation in populations exposed to hot temperature were highly accurate within, but inaccurate between, genetic backgrounds. These results seem best explained by an increased importance of epistasis during adaptation to heat and imply that the same biophysical mechanisms that increase the repeatability of phenotypic evolution by exerting strong selection at hot temperature, reduce repeatability at the genome level. Thus, predictions of adaptation in key phenotypes from genomic data may become increasingly difficult as climates warm.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"37 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264472","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Context- and sex-dependent links between sire sexual success and offspring pathogen resistance","authors":"Aijuan Liao, Tadeusz J. Kawecki","doi":"10.1101/2024.09.10.611971","DOIUrl":"https://doi.org/10.1101/2024.09.10.611971","url":null,"abstract":"Sexual selection has been proposed to promote genetic variants that improve resistance to pathogens (a special case of the \"good genes\" hypothesis). Yet, experimental tests of this hypothesis are scarce and equivocal. It is often assumed that additive genetic correlation between sexual traits and pathogen resistance is generated by their shared dependence on genetically variable \"condition\" of the organism. However, an alternative scenario posits condition-independent genetic variation in pathogen resistance; individuals more resistant to currently prevalent pathogens remain healthier and can invest more in sexual traits, but this advantage disappears in the absence of pathogens. Here, we tested whether Drosophila melanogaster males that are more sexually competitive (in terms of paternity share) sire offspring that are more resistant to the fungal pathogen Metarhizium brunneum. Furthermore, to investigate the importance of epidemiological context, we exposed sires to either an infection or a sham treatment before mating, to test whether the sire-offspring relationship depends on the presence of pathogens during sexual selection. We found that the relationship between sires sexual success and offspring pathogen resistance not only depended on sires exposure to the pathogen, but also on offspring sex. Sires that were more sexually successful in the absence of the pathogen had less resistant offspring whereas no relationship was detected for sires that competed for paternity after pathogen exposure. For daughters, the relationship tended to be negative irrespective of sire pathogen exposure. In no case was a positive correlation predicted by the \"good genes\" hypothesis detected. Thus, while sexual selection may act on genes affecting resistance in a context- and sex-dependent manner, we found no circumstances under which it promoted resistance.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"105 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264671","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Apparent timescaling of fossil diversification rates is caused by sampling bias","authors":"Bouwe Rutger Reijenga, Roger Adam Close","doi":"10.1101/2024.09.11.612481","DOIUrl":"https://doi.org/10.1101/2024.09.11.612481","url":null,"abstract":"Negative scaling relationships between both speciation and extinction rates on the one hand, and the age or duration of organismal groups on the other, are pervasive and recovered in both molecular phylogenetic and fossil time series. The consistency between molecular and fossil data hints at a universal cause, and potentially to incongruence between micro- and macroevolution. However, the existence of negative rate scaling in fossil time series has not undergone the same level of scrutiny as in molecular data. Here, we analyse the marine fossil record across the last ~535 Ma of the Phanerozoic to investigate the presence and strength of negative rate scaling. We find that negative rate scaling arises under commonly applied age range-based per-capita rates, which do not control for sampling bias, but are severely reduced or absent when metrics are used that do correct for sampling. We further show by simulation that even moderate incomplete sampling of species occurrences through time may induce rate scaling. We thus conclude that there are no significant scaling relationships present in these fossil clades, and that any apparent trend is caused by taxonomic practices and sampling artefacts. If rate scaling appears genuinely in molecular phylogenies, the absence of such a relationship in the fossil record will provide a valuable benchmark and constraint on what processes can cause it.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"8 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264676","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Mathilda Whittle, Antoine MG Barreaux, Lee R Haines, Michael B Bonsall, Sinead English, Fleur Ponton
{"title":"How does host age and nutrition affect density regulation of obligate versus facultative bacterial symbionts? Insights from the tsetse fly","authors":"Mathilda Whittle, Antoine MG Barreaux, Lee R Haines, Michael B Bonsall, Sinead English, Fleur Ponton","doi":"10.1101/2024.09.13.612807","DOIUrl":"https://doi.org/10.1101/2024.09.13.612807","url":null,"abstract":"The relationships between insect hosts and their symbionts can vary tremendously in the extent to which hosts depend on and control their symbionts. Obligate symbionts that provide micronutrients to their host are often compartmentalised to specialised host organs and depend on their hosts for survival, whereas facultative symbionts retain the ability to survive outside of their hosts. Few studies compare the extent to which a host controls and adjusts the density of obligate and facultative symbionts directly. Here, we used tsetse as a model for teasing apart the relationships between a host (Glossina morsitans morsitans) and obligate (Wigglesworthia glossinidia) and facultative (Sodalis glossinidius) symbionts. We hypothesised that tsetse actively regulate the density of Wigglesworthia according to the host's requirements, depending on their current nutritional state and developmental age. In contrast, we postulated that Sodalis retains some independence from host control, and that the growth of this symbiont is dependent on the conditions of the immediate environment, such as nutrient availability. Using qPCR, we examined how symbiont densities change across host age and the hunger cycle. Additionally, we investigated how host nutrition influences symbiont density, by comparing tsetse that were fed diluted blood (poor nutrition) or blood supplemented with yeast extract (vitamin enriched). We found that the density of Wigglesworthia did not reflect the nutritional status of the host, but was optimised to accommodate long-term host requirements (in terms of nutrient provisioning). In contrast, the density of facultative Sodalis was influenced by the ecological context (i.e. nutrient availability). This suggests that tsetse regulate the abundance of Wigglesworthia to a greater extent than Sodalis. We propose that tsetse exert only partial control over Sodalis growth due to the relatively recent transition of this symbiont to host-associated living.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"19 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264669","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Timing of starvation determines its effects on susceptibility to infection in Drosophila melanogaster females independent of host evolutionary history","authors":"Aabeer Basu, Aparajita Singh, Nagaraj Guru Prasad","doi":"10.1101/2024.09.11.612402","DOIUrl":"https://doi.org/10.1101/2024.09.11.612402","url":null,"abstract":"An organism's susceptibility to pathogens is contingent on various environmental factors, including the availability of nutrition. Starvation can alter host susceptibility to infections, either directly via depletion of resources essential for proper functioning of the immune system, or indirectly via the various physiological changes it induces within the host body. We tested if the susceptibility of Drosophila melanogaster populations to Enterococcus faecalis infection is affected by (a) whether the hosts are starved before or after the infection, and (b) the evolutionary history of the host. Hosts from laboratory fly populations that have been experimentally evolved to be more resistant to E. faecalis, and their corresponding control populations, were subjected to infection with or without being starved prior to and after being infected. We found that the effect of starvation on susceptibility to E. faecalis changed with the timing of starvation: starvation after infection improved survival of infected hosts, irrespective of how they were treated before infection, while starving only prior to infection (and not after) compromised post-infection survival. The changes in infection susceptibility were uniform in both the evolved and the control populations, suggesting that the effects of starvation are not dependent on pre-existing resistance to the infecting pathogen.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"21 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264672","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"A Newborn F-box Gene Blocks Gene Flow by Selectively Degrading Phosphoglucomutase in Species Hybrids","authors":"Dongying Xie, Yiming Ma, Pohao Ye, Yiqing Liu, Qiutao Ding, Gefei Huang, Marie-Anne Felix, Zongwei Cai, Zhongying Zhao","doi":"10.1101/2024.09.11.612556","DOIUrl":"https://doi.org/10.1101/2024.09.11.612556","url":null,"abstract":"The establishment of reproductive barriers such as postzygotic hybrid incompatibility (HI) remains the key to speciation. Gene duplication followed by differential functionalization has long been proposed as a major model underlying HI, but few supporting evidence exists. Here, we demonstrate that a new-born F-box gene, Cni-neib-1, of the nematode Caenorhabditis nigoni specifically inactivates an essential phosphoglucomutase encoded by Cbr-shls-1 in its sister species C. briggsae and their hybrids. Zygotic expression of Cni-neib-1 specifically depletes Cbr-SHLS-1, but not Cni-SHLS-1, in approximately 40 minutes starting from gastrulation, causing embryonic death. Cni-neib-1 is one of thirty-three paralogues emerging from a recent surge in F-box gene duplication events within C. nigoni, all of which are evolving under positive selection. Cni-neib-1 undergoes turnover even among C. nigoni populations. Differential expansion of F-box genes between the two species could reflect their distinctive innate immune responses. Collectively, we demonstrate how recent duplication of genes involved in protein degradation can cause unintended destruction of targets in hybrids that leads to HI, providing an invaluable insight into mechanisms of speciation.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"19 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264674","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sohini Guha, Regina B Bledsoe, Jeremy Sutherland, Brendan Epstein, Gwendolyn M Fry, Nevin Dale Young, Peter Tiffin, Liana Twardosz Burghardt
{"title":"In multi-strain inoculations, mutation of Medicago symbiosis genes creates a complex selective landscape for naturally-occurring genetic variation in rhizobia","authors":"Sohini Guha, Regina B Bledsoe, Jeremy Sutherland, Brendan Epstein, Gwendolyn M Fry, Nevin Dale Young, Peter Tiffin, Liana Twardosz Burghardt","doi":"10.1101/2024.09.11.612462","DOIUrl":"https://doi.org/10.1101/2024.09.11.612462","url":null,"abstract":"In the mutualism between leguminous plants and rhizobia bacteria, rhizobia live inside root nodules, creating the potential for host genes to shape the rhizobial selective environment. Single-strain screens have identified many host genes influencing symbiosis. However, it's unknown whether these genes influence which rhizobial strains colonize and thrive inside nodules during multi-strain inoculations. In this study, we inoculated 18 Medicago truncatula symbiotic mutants (including mutations that alter NCR peptide production, plant defence, and nodule number regulation) with a mixture of 86 Sinorhizobium meliloti strains. In multi-strain inoculations, most mutations led to reduced host benefits but widely varying effects on host investment and rhizobial benefit (i.e., strain relative fitness), revealing widespread host gene by strain fitness interactions. Genome-wide association studies identify genetic variants on rhizobial replicons pSymA and pSymB as important in mediating strain fitness responses to host mutations. While most top variants only affected rhizobial fitness when one host gene was disrupted, we identified ten variant groups with pervasive effects across six or more host mutations. These variants occurred primarily on pSymA, the symbiotic replicon, and include fixL and a few metabolic genes. In contrast to the limited-effect variants, variants with pervasive positive effects in mutants tended to adversely affect strain fitness in wild-type hosts. Our results reveal how host symbiosis genes perturb the selective landscape and symbiotic outcomes for rhizobia and set the stage for improving rhizobial inoculants and breeding legume hosts better adapted for multi-strain environments.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"100 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264675","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Aude Noiret, Agnes Lewden, Camille Lemonnier, Celine Bocquet, Marine Montblanc, Fabrice Bertile, Marine Hoareau, Elsa Marcon, Jean-Patrice Robin, Vincent A Viblanc, Antoine Stier
{"title":"Mind the polar sun: Solar radiations trigger frequent heat stress in breeding king penguins, despite relatively cool air temperatures.","authors":"Aude Noiret, Agnes Lewden, Camille Lemonnier, Celine Bocquet, Marine Montblanc, Fabrice Bertile, Marine Hoareau, Elsa Marcon, Jean-Patrice Robin, Vincent A Viblanc, Antoine Stier","doi":"10.1101/2024.09.09.611977","DOIUrl":"https://doi.org/10.1101/2024.09.09.611977","url":null,"abstract":"Polar and sub-polar animals evolved to thrive in cold climates and may thus be particularly vulnerable to the rising temperatures associated with climate change. Polar and sub-polar penguins may be especially vulnerable due to their dual habitat, alternating between foraging in cold waters and breeding/moulting on an increasingly warm land. Here, we characterized heat stress occurrence in breeding king penguins through behavioural observations and subcutaneous body temperature measurements. We show that heat stress is frequent (> 20% of observations at mid-day) in king penguins breeding in the sub-Antarctic region, and that thermoregulatory mechanisms appear insufficient to maintain stable sub-cutaneous temperature. Air temperature alone was a poor predictor of heat stress occurrence, while the combination of high solar radiations, low wind speed and high temperatures was its best predictor. Importantly, reproductive failure occurred on days warmer than average, suggesting potential significant sublethal effects of heat stress being likely to affect population dynamics.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"63 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142205370","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}