Pub Date : 2024-08-07DOI: 10.1101/2024.03.27.587025
Zahraa Al-Tameemi, Alejandra Rodriguez-Verdugo
Microbial communities are incredibly diverse. Yet, the eco-evolutionary processes originating and maintaining this diversity remain understudied. Here, we investigate the patterns of diversification for Pseudomonas putida evolving in isolation and with Acinetobacter johnsonii leaking resources used by P. putida. We experimentally evolved four experimental replicates in monoculture and co-culture for 200 generations. We observed that P. putida diversified into two distinct morphotypes that differed from their ancestor by single-point mutations. One of the most prominent mutations hit the fleQ gene encoding the master regulator of flagella and biofilm formation. We experimentally confirmed that fleQ mutants were unable to swim and formed less biofilm than their ancestor, but they also produced higher yields. Interestingly, the fleQ genotype and other mutations swept to fixation in monocultures but not in co-cultures. In co-cultures, the two lineages stably coexisted for approximately 150 generations. We hypothesized that A. johnsonii modulates the coexistence of the two lineages through frequency-dependent selection. However, invasion experiments with two genotypes in monoculture and co-culture did not support this hypothesis. Instead, we found that, at the population level, the two morphotypes coexisted at similar relative abundances in the presence of A. johnsonii whereas, in its absence, one of the morphotypes was overrepresented in the population. Overall, our study suggests that interspecies interactions play an important role in shaping patterns of diversification in microbial communities.
{"title":"Microbial diversification is maintained in an experimentally evolved synthetic community","authors":"Zahraa Al-Tameemi, Alejandra Rodriguez-Verdugo","doi":"10.1101/2024.03.27.587025","DOIUrl":"https://doi.org/10.1101/2024.03.27.587025","url":null,"abstract":"Microbial communities are incredibly diverse. Yet, the eco-evolutionary processes originating and maintaining this diversity remain understudied. Here, we investigate the patterns of diversification for <em>Pseudomonas putida</em> evolving in isolation and with <em>Acinetobacter johnsonii</em> leaking resources used by <em>P. putida</em>. We experimentally evolved four experimental replicates in monoculture and co-culture for 200 generations. We observed that <em>P. putida</em> diversified into two distinct morphotypes that differed from their ancestor by single-point mutations. One of the most prominent mutations hit the <em>fleQ</em> gene encoding the master regulator of flagella and biofilm formation. We experimentally confirmed that <em>fleQ</em> mutants were unable to swim and formed less biofilm than their ancestor, but they also produced higher yields. Interestingly, the <em>fleQ</em> genotype and other mutations swept to fixation in monocultures but not in co-cultures. In co-cultures, the two lineages stably coexisted for approximately 150 generations. We hypothesized that <em>A. johnsonii</em> modulates the coexistence of the two lineages through frequency-dependent selection. However, invasion experiments with two genotypes in monoculture and co-culture did not support this hypothesis. Instead, we found that, at the population level, the two morphotypes coexisted at similar relative abundances in the presence of <em>A. johnsonii</em> whereas, in its absence, one of the morphotypes was overrepresented in the population. Overall, our study suggests that interspecies interactions play an important role in shaping patterns of diversification in microbial communities.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"58 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938270","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}
Pub Date : 2024-08-07DOI: 10.1101/2024.08.05.606716
Warren M. Meyers, Geoffrey L. Hammond
In lower mammals testicular sex hormone-binding globulin (SHBG), also known as androgen binding protein, is well known to be a product of the Sertoli cells. However in humans, testicular SHBG is a product of the germ cells, is expressed from an upstream promoter and contains an alternative first exon 1A. Examination of testicular SHBG transcripts from members across primate suborders revealed that transcripts containing exon 1A are unique to Hominoids and Old World Monkeys. In contrast testicular SHBG transcripts in gray mouse lemur contained the proximal exon 1, while no evidence for SHBG expression could be detected in marmoset monkey testes. In general, the exonic identity of primate testicular SHBG transcripts could be predicted based on the structure of their gene’s 5’ regulatory region and we show that they change through the primate clade. This work provides insights into how molecular evolution of higher primate SHBG genes has resulted in distinct changes in how it is expressed in their testes.
{"title":"Evolution of sex hormone-binding globulin gene expression in the primate testis","authors":"Warren M. Meyers, Geoffrey L. Hammond","doi":"10.1101/2024.08.05.606716","DOIUrl":"https://doi.org/10.1101/2024.08.05.606716","url":null,"abstract":"In lower mammals testicular sex hormone-binding globulin (SHBG), also known as androgen binding protein, is well known to be a product of the Sertoli cells. However in humans, testicular SHBG is a product of the germ cells, is expressed from an upstream promoter and contains an alternative first exon 1A. Examination of testicular <em>SHBG</em> transcripts from members across primate suborders revealed that transcripts containing exon 1A are unique to Hominoids and Old World Monkeys. In contrast testicular <em>SHBG</em> transcripts in gray mouse lemur contained the proximal exon 1, while no evidence for <em>SHBG</em> expression could be detected in marmoset monkey testes. In general, the exonic identity of primate testicular <em>SHBG</em> transcripts could be predicted based on the structure of their gene’s 5’ regulatory region and we show that they change through the primate clade. This work provides insights into how molecular evolution of higher primate <em>SHBG</em> genes has resulted in distinct changes in how it is expressed in their testes.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"92 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938265","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}
Pub Date : 2024-08-07DOI: 10.1101/2024.08.05.606710
Caesar A. De La Fuente, Nehme Lahoud, Justin R. Meyer
Bacteriophages, the most abundant and genetically diverse life forms, seemingly defy fundamental ecological theory by exhibiting greater diversity than their numerous bacterial prey. This paradox raises questions about the mechanisms underlying parasite diversity. To investigate this, we took advantage of a surprising experimental result: when bacteriophage λ is continually supplied a single host, λ repeatedly evolves multiple genotypes within the same flask that vary in their receptor use. Measurements of negative frequency-dependent selection between receptor specialists revealed that diversifying selection drove their evolution and maintenance. However, the source of environmental heterogeneity necessary to generate this type of selection was unclear, as only a single isogenic host was provided and replenished every eight hours. Our experiments showed that selection for different specialist phages oscillated over the 8-hour incubation period, mirroring oscillations in gene expression of λ’s two receptors (Escherichia coli outer membrane proteins LamB and OmpF). These receptor expression changes were attributed to both cell-to-cell variation in receptor expression and rapid bacterial evolution, which we documented using phenotypic resistance assays and population genome sequencing. Our findings suggest that cryptic phenotypic variation in hosts, arising from non-genetic phenotypic heterogeneity and rapid evolution, may play a key role in driving viral diversity.
{"title":"Cryptic host phenotypic heterogeneity drives diversification of bacteriophage λ","authors":"Caesar A. De La Fuente, Nehme Lahoud, Justin R. Meyer","doi":"10.1101/2024.08.05.606710","DOIUrl":"https://doi.org/10.1101/2024.08.05.606710","url":null,"abstract":"Bacteriophages, the most abundant and genetically diverse life forms, seemingly defy fundamental ecological theory by exhibiting greater diversity than their numerous bacterial prey. This paradox raises questions about the mechanisms underlying parasite diversity. To investigate this, we took advantage of a surprising experimental result: when bacteriophage λ is continually supplied a single host, λ repeatedly evolves multiple genotypes within the same flask that vary in their receptor use. Measurements of negative frequency-dependent selection between receptor specialists revealed that diversifying selection drove their evolution and maintenance. However, the source of environmental heterogeneity necessary to generate this type of selection was unclear, as only a single isogenic host was provided and replenished every eight hours. Our experiments showed that selection for different specialist phages oscillated over the 8-hour incubation period, mirroring oscillations in gene expression of λ’s two receptors (<em>Escherichia coli</em> outer membrane proteins LamB and OmpF). These receptor expression changes were attributed to both cell-to-cell variation in receptor expression and rapid bacterial evolution, which we documented using phenotypic resistance assays and population genome sequencing. Our findings suggest that cryptic phenotypic variation in hosts, arising from non-genetic phenotypic heterogeneity and rapid evolution, may play a key role in driving viral diversity.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"15 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938273","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}
Pub Date : 2024-08-06DOI: 10.1101/2024.08.04.606548
Julian M Wagner, Jason H Wong, Jocelyn G Millar, Enes Haxhimali, Adrian Bruckner, Thomas H Naragon, James Q Boedicker, Joseph Parker
Insect diversification has been catalyzed by widespread specialization on novel hosts - a process underlying exceptional radiations of phytophagous beetles, lepidopterans, parasitoid wasps, and inordinate lineages of symbionts, predators and other trophic specialists. The strict fidelity of many such interspecies associations is posited to hinge on sensory tuning to host-derived cues, a model supported by studies of neural function in host-specific model species. Here, we investigated the sensory basis of symbiotic interactions between a myrmecophile rove beetle and its single, natural host ant species. We show that host cues trigger analogous behaviors in both ant and symbiont. Cuticular hydrocarbons - the ant's nestmate recognition pheromones - elicit partner recognition by the beetle and execution of ant grooming behavior, integrating the beetle into the colony via chemical mimicry. The beetle also follows host trail pheromones, permitting inter-colony dispersal. Remarkably, the rove beetle also performs its symbiotic behaviors with ant species separated by ~95 million years, and shows minimal preference for its natural host over non-host ants. Experimentally validated agent-based modeling supports a scenario in which specificity is enforced by physiological constraints on symbiont dispersal, and negative fitness interactions with alternative hosts, rather than via sensory tuning. Enforced specificity may be a pervasive mechanism of host range restriction of specialists embedded within host niches. Chance realization of latent compatibilities with alternative hosts may facilitate host switching, enabling deep-time persistence of obligately symbiotic lineages.
{"title":"Enforced specificity of an animal symbiosis","authors":"Julian M Wagner, Jason H Wong, Jocelyn G Millar, Enes Haxhimali, Adrian Bruckner, Thomas H Naragon, James Q Boedicker, Joseph Parker","doi":"10.1101/2024.08.04.606548","DOIUrl":"https://doi.org/10.1101/2024.08.04.606548","url":null,"abstract":"Insect diversification has been catalyzed by widespread specialization on novel hosts - a process underlying exceptional radiations of phytophagous beetles, lepidopterans, parasitoid wasps, and inordinate lineages of symbionts, predators and other trophic specialists. The strict fidelity of many such interspecies associations is posited to hinge on sensory tuning to host-derived cues, a model supported by studies of neural function in host-specific model species. Here, we investigated the sensory basis of symbiotic interactions between a myrmecophile rove beetle and its single, natural host ant species. We show that host cues trigger analogous behaviors in both ant and symbiont. Cuticular hydrocarbons - the ant's nestmate recognition pheromones - elicit partner recognition by the beetle and execution of ant grooming behavior, integrating the beetle into the colony via chemical mimicry. The beetle also follows host trail pheromones, permitting inter-colony dispersal. Remarkably, the rove beetle also performs its symbiotic behaviors with ant species separated by ~95 million years, and shows minimal preference for its natural host over non-host ants. Experimentally validated agent-based modeling supports a scenario in which specificity is enforced by physiological constraints on symbiont dispersal, and negative fitness interactions with alternative hosts, rather than via sensory tuning. Enforced specificity may be a pervasive mechanism of host range restriction of specialists embedded within host niches. Chance realization of latent compatibilities with alternative hosts may facilitate host switching, enabling deep-time persistence of obligately symbiotic lineages.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"92 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938405","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}
Pub Date : 2024-08-06DOI: 10.1101/2024.08.03.606486
Tymofii Sokolskyi, Sydney Gargulak, Esau Allen, David Baum
A key question in origins-of-life research, is whether heritability, and thus evolution, could have preceded genes. While theoretical research has shown that out of equilibrium chemical reaction networks with multiple autocatalytic motifs can provide chemical “memory” and serve as units of heritability, experimental validation is lacking. We established conditions that may be conducive to these processes and developed methods to seek evidence of heritability. We prepared a food set (FS) of three small organic species (methanol, formic acid, and acetic acid), three inorganic salts (sodium trimetaphosphate, ammonium hydroxide, sodium bicarbonate), and pyrite mineral. We conducted a serial dilution experiment where FS was assembled, autoclaved, and the incubated for 24 hours, after which a 20% fraction was transferred into freshly prepared FS that went through the same procedure. This process was repeated for 10 transfer (TR) generations. To serve as controls, we also incubated the fresh solutions in each generation. Over the course of the experiment, we compared the chemical composition of transfer (TR) vials and no-transfer control (NTC) vials using liquid chromatography-mass spectrometry (LCMS). We adapted metrics from ecology and evolutionary biology to analyze the chemical composition data, finding a great deal of variability. Nonetheless, by focusing on a subset of the chemicals with more consistent patterns, we found evidence of heritable variation among vials.
{"title":"Measuring heritability in messy prebiotic chemical systems","authors":"Tymofii Sokolskyi, Sydney Gargulak, Esau Allen, David Baum","doi":"10.1101/2024.08.03.606486","DOIUrl":"https://doi.org/10.1101/2024.08.03.606486","url":null,"abstract":"A key question in origins-of-life research, is whether heritability, and thus evolution, could have preceded genes. While theoretical research has shown that out of equilibrium chemical reaction networks with multiple autocatalytic motifs can provide chemical “memory” and serve as units of heritability, experimental validation is lacking. We established conditions that may be conducive to these processes and developed methods to seek evidence of heritability. We prepared a food set (FS) of three small organic species (methanol, formic acid, and acetic acid), three inorganic salts (sodium trimetaphosphate, ammonium hydroxide, sodium bicarbonate), and pyrite mineral. We conducted a serial dilution experiment where FS was assembled, autoclaved, and the incubated for 24 hours, after which a 20% fraction was transferred into freshly prepared FS that went through the same procedure. This process was repeated for 10 transfer (TR) generations. To serve as controls, we also incubated the fresh solutions in each generation. Over the course of the experiment, we compared the chemical composition of transfer (TR) vials and no-transfer control (NTC) vials using liquid chromatography-mass spectrometry (LCMS). We adapted metrics from ecology and evolutionary biology to analyze the chemical composition data, finding a great deal of variability. Nonetheless, by focusing on a subset of the chemicals with more consistent patterns, we found evidence of heritable variation among vials.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"37 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141969037","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}
Pub Date : 2024-08-06DOI: 10.1101/2024.08.02.606322
Thomas D. Lewin, Isabel Jiah-Yih Liao, Yi-Jyun Luo
Species from diverse animal lineages, including molluscs, hemichordates, and chordates, have retained groups of orthologous genes on the same chromosomes for over half a billion years since the last common ancestor of bilaterians. Though there are notable exceptions, it has been proposed that the conservation of chromosome-scale gene linkages is the norm among animals. Here, by examining interchromosomal rearrangements in 64 chromosome-level genomes across 15 bilaterian phyla and at least 52 classes, we show that cases of genome structure conservation are exceptionally rare. Large-scale genome restructuring events correlate with increased rates of protein sequence evolution and may represent a previously underappreciated contributor to adaptation and animal diversity.
{"title":"Conservation of animal genome structure is the exception not the rule","authors":"Thomas D. Lewin, Isabel Jiah-Yih Liao, Yi-Jyun Luo","doi":"10.1101/2024.08.02.606322","DOIUrl":"https://doi.org/10.1101/2024.08.02.606322","url":null,"abstract":"Species from diverse animal lineages, including molluscs, hemichordates, and chordates, have retained groups of orthologous genes on the same chromosomes for over half a billion years since the last common ancestor of bilaterians. Though there are notable exceptions, it has been proposed that the conservation of chromosome-scale gene linkages is the norm among animals. Here, by examining interchromosomal rearrangements in 64 chromosome-level genomes across 15 bilaterian phyla and at least 52 classes, we show that cases of genome structure conservation are exceptionally rare. Large-scale genome restructuring events correlate with increased rates of protein sequence evolution and may represent a previously underappreciated contributor to adaptation and animal diversity.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"371 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938271","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}
Pub Date : 2024-08-06DOI: 10.1101/2024.08.06.606888
Vivaswat Shastry, Jeremy J. Berg
For many problems in population genetics, it is useful to characterize the distribution of fitness effects (DFE) of de novo mutations among a certain class of sites. A DFE is typically estimated by fitting an observed site frequency spectrum (SFS) to an expected SFS given a hypothesized distribution of selection coefficients and demographic history. The development of tools to infer gene trees from haplotype alignments, along with ancient DNA resources, provides us with additional information about the frequency trajectories of segregating mutations. Here, we ask how useful this additional information is for learning about the DFE, using the joint distribution on allele frequency and age to summarize information about the trajectory. To this end, we introduce an accurate and efficient numerical method for computing the density on the age of a segregating variant found at a given sample frequency, given the strength of selection and an arbitrarily complex population size history. We then use this framework to show that the unconditional age distribution of negatively selected alleles is very closely approximated by re-weighting the neutral age distribution in terms of the negatively selected SFS, suggesting that allele ages provide very little information about the DFE beyond that already contained in the present day frequency. To confirm this prediction, we extended the standard Poisson Random Field (PRF) method to incorporate the joint distribution of frequency and age in estimating selection coefficients, and test its performance using simulations. We find that when the full SFS is observed and the true allele ages are known, including ages in the estimation provides only small increases in the accuracy of estimated selection coefficients. However, if only sites with frequencies above a certain threshold are observed, then the true ages can provide substantial information about the selection coefficients, especially when the selection coefficient is large. When ages are estimated from haplotype data using state-of-the-art tools, uncertainty about the age abrogates most of the additional information in the fully observed SFS case, while the neutral prior assumed in these tools when estimating ages induces a downward bias in the case of the thresholded SFS.
{"title":"Allele ages provide limited information about the strength of negative selection","authors":"Vivaswat Shastry, Jeremy J. Berg","doi":"10.1101/2024.08.06.606888","DOIUrl":"https://doi.org/10.1101/2024.08.06.606888","url":null,"abstract":"For many problems in population genetics, it is useful to characterize the distribution of fitness effects (DFE) of <em>de novo</em> mutations among a certain class of sites. A DFE is typically estimated by fitting an observed site frequency spectrum (SFS) to an expected SFS given a hypothesized distribution of selection coefficients and demographic history. The development of tools to infer gene trees from haplotype alignments, along with ancient DNA resources, provides us with additional information about the frequency trajectories of segregating mutations. Here, we ask how useful this additional information is for learning about the DFE, using the joint distribution on allele frequency and age to summarize information about the trajectory. To this end, we introduce an accurate and efficient numerical method for computing the density on the age of a segregating variant found at a given sample frequency, given the strength of selection and an arbitrarily complex population size history. We then use this framework to show that the unconditional age distribution of negatively selected alleles is very closely approximated by re-weighting the neutral age distribution in terms of the negatively selected SFS, suggesting that allele ages provide very little information about the DFE beyond that already contained in the present day frequency. To confirm this prediction, we extended the standard Poisson Random Field (PRF) method to incorporate the joint distribution of frequency and age in estimating selection coefficients, and test its performance using simulations. We find that when the full SFS is observed and the true allele ages are known, including ages in the estimation provides only small increases in the accuracy of estimated selection coefficients. However, if only sites with frequencies above a certain threshold are observed, then the true ages can provide substantial information about the selection coefficients, especially when the selection coefficient is large. When ages are estimated from haplotype data using state-of-the-art tools, uncertainty about the age abrogates most of the additional information in the fully observed SFS case, while the neutral prior assumed in these tools when estimating ages induces a downward bias in the case of the thresholded SFS.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"47 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938406","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}
Pub Date : 2024-08-06DOI: 10.1101/2024.08.01.605096
Holger Herlyn, Anju Angelina Hembrom, Juan Pablo Tosar, Katharina M Mauer, Hanno Schmidt, Bahram Sayyaf Dezfuli, Thomas Hankeln, Lutz Bachmann, Peter Sarkies, Kevin J Peterson, Bastian Fromm
During the last 800 million years of evolution animals radiated into a vast range of diversity of species and disparity of forms and lifestyles. The process involved a near hierarchical increase in complexity from life forms with few cell types to organisms with many hundreds of cell-types. However, neither genome size nor number of protein-coding genes can explain these differences and their biological basis remains elusive. Yet, recent studies have suggested that the evolution of complexity is closely linked to the acquisition of a class of protein coding gene-regulators called microRNAs. In a regressive approach, to investigate the association between loss of organismal complexity and microRNAs, we here studied Syndermata, an invertebrate group including free-living rotifers (Monogononta, Bdelloidea), the epibiotic Seisonidea and the endoparasitic Acanthocephala. Genomic, transcriptomic and morphological characterization and comparisons across 25 syndermatan species revealed a strong correlation between loss of microRNAs, loss of protein-coding genes and decreasing morphological complexity. The near hierarchical loss extends to ~85% loss of microRNAs and a ~50% loss of BUSCO genes in the endoparasitic Acanthocephala, the most reduced group we studied. Together, the loss of ~400 protein-coding genes and ~10 metazoan core gene losses went along with one microRNA family loss. Furthermore, the loss of ~4 microRNA families or ~34 metazoan core genes associated with one lost morphological feature. These are the first quantitative insights into the regulatory impact of microRNAs on organismic complexity as a predictable consequence in regressive evolution of parasites.
{"title":"Substantial hierarchical reductions of genetic and morphological traits in the evolution of rotiferan parasites","authors":"Holger Herlyn, Anju Angelina Hembrom, Juan Pablo Tosar, Katharina M Mauer, Hanno Schmidt, Bahram Sayyaf Dezfuli, Thomas Hankeln, Lutz Bachmann, Peter Sarkies, Kevin J Peterson, Bastian Fromm","doi":"10.1101/2024.08.01.605096","DOIUrl":"https://doi.org/10.1101/2024.08.01.605096","url":null,"abstract":"During the last 800 million years of evolution animals radiated into a vast range of diversity of species and disparity of forms and lifestyles. The process involved a near hierarchical increase in complexity from life forms with few cell types to organisms with many hundreds of cell-types. However, neither genome size nor number of protein-coding genes can explain these differences and their biological basis remains elusive. Yet, recent studies have suggested that the evolution of complexity is closely linked to the acquisition of a class of protein coding gene-regulators called microRNAs. In a regressive approach, to investigate the association between loss of organismal complexity and microRNAs, we here studied Syndermata, an invertebrate group including free-living rotifers (Monogononta, Bdelloidea), the epibiotic Seisonidea and the endoparasitic Acanthocephala. Genomic, transcriptomic and morphological characterization and comparisons across 25 syndermatan species revealed a strong correlation between loss of microRNAs, loss of protein-coding genes and decreasing morphological complexity. The near hierarchical loss extends to ~85% loss of microRNAs and a ~50% loss of BUSCO genes in the endoparasitic Acanthocephala, the most reduced group we studied. Together, the loss of ~400 protein-coding genes and ~10 metazoan core gene losses went along with one microRNA family loss. Furthermore, the loss of ~4 microRNA families or ~34 metazoan core genes associated with one lost morphological feature. These are the first quantitative insights into the regulatory impact of microRNAs on organismic complexity as a predictable consequence in regressive evolution of parasites.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"15 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141968953","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}
Pub Date : 2024-08-06DOI: 10.1101/2024.08.02.606438
Diana Aguilar-Gómez, Layla Freeborn, Lin Yuan, Lydia L. Smith, Alex Guzman, Andrew H. Vaughn, Emma Steigerwald, Adam Stuckert, Yusan Yang, Tyler Linderoth, Matthew MacManes, Corinne Richards-Zawacki, Rasmus Nielsen
The aposematic strawberry poison frog, Oophaga pumilio, is an iconic model system for studying the evolution and maintenance of color variation. Through most of its range, this frog is red with blue limbs. However, frogs from the Bocas del Toro Province, Panama, show striking variance in color and pattern, both sympatrically and allopatrically. This observation contradicts standard models of the evolution of aposematism and has led to substantial speculation about its evolutionary and molecular causes. Since the enigma of O. pumilio phenotypic variation is partly unresolved because of its large, ∼ 6.7 Gb genome, we here sequence exomes from 347 individuals from ten populations and map a number of genetic factors responsible for the color and pattern variation. The kit gene is the primary candidate underlying the blue-red polymorphism in Dolphin Bay, where an increase in melanosomes is correlated with blue coloration. Additionally, the ttc39b gene, a known enhancer of yellow-to-red carotenoid conversion in birds, is the primary factor behind the yellow-red polymorphism in the Bastimentos West area. The causal genetic regions show evidence of selective sweeps acting locally to spread the rare phenotype. Our analyses suggest an evolutionary model in which selection is driving the formation of new morphs in a dynamic system resulting from a trade-off between predation avoidance, intraspecific competition, and mate choice.
{"title":"Evolution and Diversification of the Aposematic Poison Frog, Oophaga pumilio, in Bocas del Toro","authors":"Diana Aguilar-Gómez, Layla Freeborn, Lin Yuan, Lydia L. Smith, Alex Guzman, Andrew H. Vaughn, Emma Steigerwald, Adam Stuckert, Yusan Yang, Tyler Linderoth, Matthew MacManes, Corinne Richards-Zawacki, Rasmus Nielsen","doi":"10.1101/2024.08.02.606438","DOIUrl":"https://doi.org/10.1101/2024.08.02.606438","url":null,"abstract":"The aposematic strawberry poison frog, <em>Oophaga pumilio</em>, is an iconic model system for studying the evolution and maintenance of color variation. Through most of its range, this frog is red with blue limbs. However, frogs from the Bocas del Toro Province, Panama, show striking variance in color and pattern, both sympatrically and allopatrically. This observation contradicts standard models of the evolution of aposematism and has led to substantial speculation about its evolutionary and molecular causes. Since the enigma of <em>O. pumilio</em> phenotypic variation is partly unresolved because of its large, ∼ 6.7 Gb genome, we here sequence exomes from 347 individuals from ten populations and map a number of genetic factors responsible for the color and pattern variation. The <em>kit</em> gene is the primary candidate underlying the blue-red polymorphism in Dolphin Bay, where an increase in melanosomes is correlated with blue coloration. Additionally, the <em>ttc39b</em> gene, a known enhancer of yellow-to-red carotenoid conversion in birds, is the primary factor behind the yellow-red polymorphism in the Bastimentos West area. The causal genetic regions show evidence of selective sweeps acting locally to spread the rare phenotype. Our analyses suggest an evolutionary model in which selection is driving the formation of new morphs in a dynamic system resulting from a trade-off between predation avoidance, intraspecific competition, and mate choice.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"31 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938407","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}
Pub Date : 2024-08-06DOI: 10.1101/2024.08.06.606803
Wei-Yun Lai, Sheng-Kai Hsu, Andreas Futschik, Christian Schlötterer
The phenomenon of parallel evolution, whereby similar genomic and phenotypic changes occur across replicated pairs of population or species, is widely studied. Nevertheless, the determining factors of parallel evolution remain poorly understood. Theoretical studies have proposed that pleiotropy, the influence of a single gene on multiple traits, is an important factor. In order to gain a deeper insight into the role of pleiotropy for parallel evolution from standing genetic variation, we characterized the interplay between parallelism, polymorphism and pleiotropy. The present study examined the parallel gene expression evolution in 10 replicated populations of Drosophila simulans, which were adapted from standing variation to the same new temperature regime. The data demonstrate that parallel evolution of gene expression from standing genetic variation is positively correlated with the strength of pleiotropic effects. The ancestral variation in gene expression is, however, negatively correlated with parallelism. Given that pleiotropy is also negatively correlated with gene expression variation, we conducted a causal analysis to distinguish cause and correlation and evaluate the role of pleiotropy. The causal analysis indicated that both direct (causative) and indirect (correlational) effects of pleiotropy contribute to parallel evolution. The indirect effect is mediated by historic selective constraint in response to pleiotropy. This results in parallel selection responses due to the reduced standing variation of pleiotropic genes. The direct effect of pleiotropy is likely to reflect a genetic correlation among adaptive traits, which in turn gives rise to synergistic effects and higher parallelism.
{"title":"Pleiotropy increases parallel selection signatures during adaptation from standing genetic variation","authors":"Wei-Yun Lai, Sheng-Kai Hsu, Andreas Futschik, Christian Schlötterer","doi":"10.1101/2024.08.06.606803","DOIUrl":"https://doi.org/10.1101/2024.08.06.606803","url":null,"abstract":"The phenomenon of parallel evolution, whereby similar genomic and phenotypic changes occur across replicated pairs of population or species, is widely studied. Nevertheless, the determining factors of parallel evolution remain poorly understood. Theoretical studies have proposed that pleiotropy, the influence of a single gene on multiple traits, is an important factor. In order to gain a deeper insight into the role of pleiotropy for parallel evolution from standing genetic variation, we characterized the interplay between parallelism, polymorphism and pleiotropy. The present study examined the parallel gene expression evolution in 10 replicated populations of <em>Drosophila simulans</em>, which were adapted from standing variation to the same new temperature regime. The data demonstrate that parallel evolution of gene expression from standing genetic variation is positively correlated with the strength of pleiotropic effects. The ancestral variation in gene expression is, however, negatively correlated with parallelism. Given that pleiotropy is also negatively correlated with gene expression variation, we conducted a causal analysis to distinguish cause and correlation and evaluate the role of pleiotropy. The causal analysis indicated that both direct (causative) and indirect (correlational) effects of pleiotropy contribute to parallel evolution. The indirect effect is mediated by historic selective constraint in response to pleiotropy. This results in parallel selection responses due to the reduced standing variation of pleiotropic genes. The direct effect of pleiotropy is likely to reflect a genetic correlation among adaptive traits, which in turn gives rise to synergistic effects and higher parallelism.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"78 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141938404","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}
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