{"title":"Polygenic barriers to sex chromosome turnover","authors":"Pavitra Muralidhar","doi":"10.1101/2024.09.03.611135","DOIUrl":"https://doi.org/10.1101/2024.09.03.611135","url":null,"abstract":"In organisms with distinct sexes, sex is commonly determined by segregation of a pair of chromosomes in paternal meiosis (male heterogamety) or maternal meiosis (female heterogamety). Evolutionary transitions between sex-chromosome systems—which change the chromosome pair that determines sex, the system of heterogamety, or both—are frequent in some clades. In others, however, sex chromosome systems show long-term stability. Previous explanations of this stasis rely on evolutionary dynamics peculiar to sex linkage, such as the accumulation of deleterious mutations on the sex-specific chromosome or sexually antagonistic mutations on either sex chromosome. Here, I show that the ordinary operation of stabilizing selection on quantitative traits can, as a by-product, promote stability of sex chromosome systems. The reason is that stabilizing selection on a trait permits individual chromosomes' genetic contributions to the trait to drift upwards or downwards, subject only to the constraint that they all sum to the trait optimum. This chromosome-specific drift causes reduced fitness in individuals with unusual chromosomal constitutions, such as the novel sexual genotypes that sex chromosome turnovers always produce. The theory can explain a suite of patterns in the phylogenetic distribution of sex determining systems. Applied to interspecific hybrids, it can also explain two key observations concerning their reduced fitness: Haldane's rule and the large-X effect.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"28 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142205484","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}
Damien Genettais, Charles Bernard, Félix Geoffroy, Clément Nizak, Sandrine Adiba
{"title":"Continuous emergence of phototaxis in Dictyostelium discoideum","authors":"Damien Genettais, Charles Bernard, Félix Geoffroy, Clément Nizak, Sandrine Adiba","doi":"10.1101/2024.08.11.607478","DOIUrl":"https://doi.org/10.1101/2024.08.11.607478","url":null,"abstract":"The evolutionary transition from uni- to multicellularity is associated with new properties resulting from collective cell behavior. The social amoeba <em>Dictyostelium discoideum</em> alternating between individual cells and multicellular forms of varying size provides a powerful biological system to characterize such emergent properties. Multicellular forms coined slugs have long been described as chemotactic towards cAMP, and also as phototactic. While chemotaxis is also well-documented at the single-cell level, which merely explains slug chemotaxis, we asked whether slug phototaxis is an emergent property of multicellularity. For this, we developed an automated microscopy setup to quantify and compare the migration trajectories of single cells and slugs moving in the dark or illuminated with lateral light. We find that single cells, either extracted from phototactic slugs or taken prior to multicellular aggregation, are not phototactic, implying that slug phototaxis results from interactions between cells that lack this property. Further, by analysing slugs composed of a varying number of cells, we find that phototaxis efficiency increases continuously with slug size. Cell-cell interactions combined with self-organization are thus key elements for this property to emerge.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"47 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938387","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}
I-Chen Kimberly Chen, Shania Khatri, Matthew D. Herron, Frank Rosenzweig
{"title":"Genetic predisposition towards multicellularity in Chlamydomonas reinhardtii","authors":"I-Chen Kimberly Chen, Shania Khatri, Matthew D. Herron, Frank Rosenzweig","doi":"10.1101/2024.08.09.607418","DOIUrl":"https://doi.org/10.1101/2024.08.09.607418","url":null,"abstract":"The evolution from unicellular to multicellular organisms facilitates further phenotypic innovations, notably cellular differentiation. Multiple research groups have shown that in the laboratory simple, obligate multicellularity can evolve from a unicellular ancestor under appropriate selection. However, little is known about the extent to which deterministic factors like ancestral genotype and environmental context influence the likelihood of this evolutionary transition. To test whether certain genotypes are predisposed to evolve multicellularity in different environments, we carried out a set of 24 evolution experiments each founded by a population consisting of 10 different strains of the unicellular green alga Chlamydomonas reinhardtii, all in equal proportions. Twelve of the initially identical replicate populations were subjected to predation by the protist Parmecium tetraurelia while the other 12 were subjected to settling selection by slow centrifugation. Population subsamples were transferred to fresh media on a weekly basis for a total of 40 transfers (~600 generations). Heritable multicellular structures arose in four of 12 predation-selected populations (6 multicellular isolates in total), but never in the settling selection populations. By comparing whole genome sequences of the founder and evolved strains, we discovered that every multicellular isolate arose from one of two founders. Cell cluster size varied not only among evolved strains derived from different ancestors but among strains derived from the same ancestor. These findings show that both deterministic and stochastic factors influence whether initially unicellular populations can evolve simple multicellular structures.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"40 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938389","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":"The double-edged effect of environmental fluctuations on evolutionary rescue","authors":"Shota Shibasaki, Masato Yamamichi","doi":"10.1101/2024.08.09.607399","DOIUrl":"https://doi.org/10.1101/2024.08.09.607399","url":null,"abstract":"Recent studies revealed that contemporary evolution can be rapid enough to prevent population extinction in deteriorating environments through \"evolutionary rescue\". Researchers have investigated how evolutionary rescue is affected by various factors such as initial population sizes, the amount of genetic variation, and the speed of environmental changes, but few studies focused on environmental fluctuations. As the ongoing global changes are influencing the mean and variance of many environmental variables, it is crucial to explore how environmental fluctuations affect evolutionary rescue for understanding eco-evolutionary dynamics in the wild. Here we show that increasing the amplitude of environmental fluctuations around long-term deteriorating trends has negative and positive effects on evolutionary rescue by analyzing a mathematical model and conducting laboratory experiments on the green alga Chlorella vulgaris under increasing salinity. Increasing the amplitude of environmental fluctuations produces an episode of a huge environmental change, thereby increasing the adaptation lag between the optimal trait value and the population trait mean, which eventually causes population extinction in model simulations. On the other hand, large environmental fluctuations can increase trait variance within a population, potentially promoting adaptive evolution. Indeed, we observed that algal strains that experienced large environmental fluctuations could grow in a harsh environment whereas strains that experienced smaller or no environmental fluctuations could not. These results suggest that we will be able to promote or prohibit evolutionary rescue in nature by carefully considering the double-edged effect of environmental fluctuations on evolutionary rescue.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"15 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141969038","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}
Shen-Ao Liang, Tianxin Ren, Jiayu Zhang, Jiahui He, Xuankai Wang, Xinrui Jiang, Yuan He, Rajiv C. McCoy, Qiaomei Fu, Joshua M. Akey, Yafei Mao, Lu Chen
{"title":"A Refined Analysis of Neanderthal-Introgressed Sequences in Modern Humans with a Complete Reference Genome","authors":"Shen-Ao Liang, Tianxin Ren, Jiayu Zhang, Jiahui He, Xuankai Wang, Xinrui Jiang, Yuan He, Rajiv C. McCoy, Qiaomei Fu, Joshua M. Akey, Yafei Mao, Lu Chen","doi":"10.1101/2024.08.09.607285","DOIUrl":"https://doi.org/10.1101/2024.08.09.607285","url":null,"abstract":"Background: Leveraging long-read sequencing technologies, the first complete human reference genome, T2T-CHM13, corrects the assembly errors in prior references and addresses the remaining 8% of the genome. While the studies on archaic admixture in modern humans so far have been relying on the GRCh37 reference due to the archaic genome data, the impact of T2T-CHM13 in this field remains unknown. Results: We remapped the sequencing reads of the high-quality Altai Neanderthal and Denisovan genomes onto GRCh38 and T2T-CHM13 respectively. Compared with GRCh37, we found T2T-CHM13 has a significant improvement of read mapping quality in archaic samples. We then applied IBDmix to identify Neanderthal introgressed sequences in 2,504 individuals from 26 geographically diverse populations in different references. We observed different pre-phasing filtering strategies prevalently used in public data can largely impact determination of archaic ancestry, calling for consideration on the choice of filters. We discovered ~51Mb T2T-CHM13 unique Neanderthal sequences, which are predominantly located in regions where the variants distinct between the GRCh38 and T2T-CHM13 assemblies emerge. Besides, we unfolded new instances of population-specific archaic introgression in diverse populations, covering genes involved in metabolism, olfactory-related, and icon-channel. Finally, we integrated the introgressed sequences and adaptive signals with all references into a visualization database website, called ASH (www.arcseqhub.com), to facilitate the utilization of archaic alleles and adaptive signals in human genomics and evolutionary research. Conclusions: Our study refines the detection of archaic variations in modern humans, highlights the importance of T2T-CHM13 reference utility, and provides novel insights into functional consequences of archaic hominin admixture.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"50 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938388","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}
Skyler Berardi, Jessica A Rhodes, Mary Catherine Berner, Sharon I Greenblum, Mark C Bitter, Emily L Behrman, Nicolas J Betancourt, Alan O Bergland, Dmitri A Petrov, Subhash Rajpurohit, Paul Schmidt
{"title":"Drosophila melanogaster pigmentation demonstrates adaptive phenotypic parallelism but genomic unpredictability over multiple timescales","authors":"Skyler Berardi, Jessica A Rhodes, Mary Catherine Berner, Sharon I Greenblum, Mark C Bitter, Emily L Behrman, Nicolas J Betancourt, Alan O Bergland, Dmitri A Petrov, Subhash Rajpurohit, Paul Schmidt","doi":"10.1101/2024.08.09.607378","DOIUrl":"https://doi.org/10.1101/2024.08.09.607378","url":null,"abstract":"Populations are capable of responding to environmental change over ecological timescales via adaptive tracking. However, the translation from patterns of allele frequency change to rapid adaptation of complex traits remains unresolved. We used abdominal pigmentation in Drosophila melanogaster as a model phenotype to address the nature, genetic architecture, and repeatability of rapid adaptation in the field. We show that D. melanogaster pigmentation evolves as a highly parallel and deterministic response to shared environmental gradients across latitude and season in natural North American populations. We then experimentally evolved replicate, genetically diverse fly populations in field mesocosms to remove any confounding effects of demography and/or cryptic structure that may drive patterns in wild populations; we show that pigmentation rapidly responds, in parallel, in fewer than ten generations. Thus, pigmentation evolves concordantly in response to spatial and temporal climatic gradients. We next examined whether phenotypic differentiation was associated with allele frequency change at loci with established links to genetic variance in pigmentation in natural populations. We found that across all spatial and temporal scales, phenotypic patterns were associated with variation at pigmentation-related loci, and the sets of genes we identified in each context were largely nonoverlapping. Therefore, our findings suggest that parallel phenotypic evolution is associated with an unpredictable genomic response, with distinct components of the polygenic architecture shifting across each environmental gradient to produce redundant adaptive patterns.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"30 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938391","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}
Michaela Zwyer, Zhi Ming Xu, Amanda Ross, Jerry Hella, Mohamed Sasamalo, Maxime Rotival, Hellen Hiza, Liliana K Rutaihwa, Klaus Reither, Jacques Fellay, Damien Portevin, Lluis Quintana-Murci, Sebastien Gagneux, Daniela Brites
{"title":"Human genetic ancestry, Mycobacterium tuberculosis diversity and tuberculosis disease severity in Dar es Salaam, Tanzania","authors":"Michaela Zwyer, Zhi Ming Xu, Amanda Ross, Jerry Hella, Mohamed Sasamalo, Maxime Rotival, Hellen Hiza, Liliana K Rutaihwa, Klaus Reither, Jacques Fellay, Damien Portevin, Lluis Quintana-Murci, Sebastien Gagneux, Daniela Brites","doi":"10.1101/2024.08.10.607244","DOIUrl":"https://doi.org/10.1101/2024.08.10.607244","url":null,"abstract":"Infectious diseases have affected humanity for millennia and are among the strongest selective forces. Tuberculosis (TB) is an ancient disease, caused by the human-adapted members of the Mycobacterium tuberculosis complex (MTBC). The outcome of TB infection and disease is highly variable, and co-evolution between human populations and their MTBC strains may account for some of this variability. Particular human genetic ancestries have been associated with higher susceptibility to TB, but socio-demographic aspects of the disease can confound such associations. Here, we studied 1,000 TB patients from Dar es Salaam, Tanzania, together with their respective MTBC isolates, by combining human and bacterial genomics with clinical data. We found that the genetic background of the TB patient population was strongly influenced by the Bantu migrations from West Africa, which is in contrast to the corresponding MTBC genotypes that were mainly introduced from outside Africa. These findings suggest a recent evolutionary history of co-existence between the human and MTBC populations in Dar es Salaam. We detected no evidence of an effect of human genetic ancestry, or MTBC phylogenetic diversity alone, nor their interaction, on TB disease severity. Treatment-seeking, social and environmental factors are likely to be the main determinants of disease severity at the point of care in this patient population.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"58 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938393","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":"The danger zone: the joint trap of incomplete lineage sorting and long-branch attraction in placing Rafflesiaceae","authors":"Liming Cai, Liang Liu, Charles C. Davis","doi":"10.1101/2024.08.07.606681","DOIUrl":"https://doi.org/10.1101/2024.08.07.606681","url":null,"abstract":"Two key factors have been implicated as major impediments to phylogenomic inference: incomplete lineage sorting (ILS)—especially in cases where clades are in the anomaly zone—and erroneous gene tree estimation—commonly manifested by long-branch attraction in the Felsenstein zone. Seldom have these factors been analyzed when they occur simultaneously as in cases involving ancient adaptive radiations. Rafflesiaceae (Malpighiales) is an iconic holoparasitic plant clade growing west of Wallace’s line in tropical Southeast Asia. This clade has been notoriously difficult to place phylogenetically and is nested within an explosive ancient radiation in Malpighiales. To complicate matters, parasitic plants like Rafflesiaceae are well-known to exhibit accelerated rates of nucleotide substitution. Here, using 2,141 genes we identify for the first time that accelerated substitution rates is a genome-wide phenomenon in holoparasites. We demonstrate two orders of magnitude increase in substitution rates in Rafflesiaceae compared to its free-living relatives, rendering nearly every gene prone to long-branch attraction. Our analyses rejected the monophyletic (Rafflesiaceae, Euphorbiaceae) clade proposed in previous studies but favored an earlier divergence of Rafflesiaceae in close affinity with Euphorbiaceae, Peraceae, Putranjivaceae, and Pandaceae. Rafflesiaceae is therefore prey to a joint trap of the anomaly and Felsenstein zones. Moreover, owing to massive gene loss within Rafflesiaceae, our simulation suggests that this represents an intractable phylogenetic problem that will never achieve a single phylogenetic resolution. Our case study highlights a seemingly insurmountable confluence of factors—a danger zone—that hinders phylogenomic resolution and demonstrates the need to be flexible in cases where multiple phylogenomic placements are equally likely.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"15 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141969878","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}
Elpida Skarlou, Fanny Laugier, Kevin Bethune, Timothee Chenin, Jean-Marc Donnay, Celine Froissard, Patrice David
{"title":"Complex genetic determination of male-fertility restoration in the gynodioecious snail Physa acuta","authors":"Elpida Skarlou, Fanny Laugier, Kevin Bethune, Timothee Chenin, Jean-Marc Donnay, Celine Froissard, Patrice David","doi":"10.1101/2024.08.08.607164","DOIUrl":"https://doi.org/10.1101/2024.08.08.607164","url":null,"abstract":"Male fertility in plants is often controlled by the interaction between mitochondrial and nuclear genes. Some mitotypes confer cytoplasmic male sterility (CMS), making the individual male-sterile, unless the nuclear background contains alleles called restorers, that suppress the effects of CMS and restore the hermaphroditic condition. Restorers in cultivated crops are often alleles with strong and dominant effect, but in wild plants, data often suggest more complex systems. Here, we characterized the inheritance and specificity of restoration in a new CMS model, the freshwater snail Physa acuta. We explored two different populations (i) a naive population i.e., without contact CMS in the past 80 generations, (ii) a non-naive population, where CMS is present and largely restored. We found that restoration potential was indeed heritable in both contexts and specific to a CMS type. However our results suggest that restoration of male fertility could be of a different nature depending on population history: in naive populations not coevolved with CMS the background variation may include alleles that happen to act as weak quantitative modifiers of the penetrance of CMS, while in populations coevolved with CMS, selection may have favored, when such variants were available, the emergence of strong alleles with a dominant effect.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"133 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938394","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}
Jacqueline J Peña, Eduardo FC Scopel, Audrey K Ward, Douda Bensasson
{"title":"Footprints of human migration in the population structure of wild wine yeast","authors":"Jacqueline J Peña, Eduardo FC Scopel, Audrey K Ward, Douda Bensasson","doi":"10.1101/2024.08.08.607167","DOIUrl":"https://doi.org/10.1101/2024.08.08.607167","url":null,"abstract":"Humans have a long history of fermenting food and beverages that led to domestication of the wine yeast, Saccharomyces cerevisiae. Despite their tight companionship with humans, yeast species that are domesticated or pathogenic can also live on trees. Here we used over 300 genomes of S. cerevisiae from oaks and other trees to determine whether tree-associated populations are genetically distinct from domesticated lineages and estimate the timing of forest lineage divergence. We found populations on trees are highly structured within Europe, Japan, and North America. Approximate estimates of when forest lineages diverged out of Asia and into North America and Europe coincide with the end of the last ice age, the spread of agriculture, and the onset of fermentation by humans. It appears that migration from human-associated environments to trees is ongoing. Indeed, patterns of ancestry in the genomes of three recent migrants from the trees of North America to Europe could be explained by the human response to the Great French Wine Blight. Our results suggest that human-assisted migration affects forest populations, albeit rarely. Such migration events may even have shaped the global distribution of S. cerevisiae. Given the potential for lasting impacts due to yeast migration between human and natural environments, it seems important to understand the evolution of human commensals and pathogens in wild niches.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"6 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938264","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}