The time needed for the evolution of mating cues that distinguish species, such as species-specific songs or plumage coloration in birds, has received little attention. Aiming to gain some understanding of the timing of the evolutionary process we here present models of how mating cues evolve in populations split into subpopulations between which there may (parapatry) or may not (allopatry) be migration. Mating cues can be either neutral or directly selected. In models in which evolution commences with a substitution at a neutral mating-cue locus, under allopatry there is no selection on the mating cue, but under parapatry selection may be induced on the mating cue by the selective conditions in the subpopulations and the migration rates between them. We use simulation to calculate how selection pressures on mating cues then depend on selective conditions in subpopulations and migration rates between them. In the second part of the paper we demonstrate quantitatively how the resulting selection pressures on new mating cues together with mutation rate affect speciation time. Our results suggest that species-specific songs or plumage colorations that are selectively neutral evolve faster under parapatry than under allopatry, and this may explain the short speciation times that are sometimes reported. Although our modelling assumptions are restrictive so that caution is needed in comparing the results to empirical data, we hope that our main results, showing quantitatively how parapatry can reduce speciation times, will encourage further work relaxing model assumptions or studying different models of mate choice.
{"title":"Times needed to evolve mating cues under allopatry and parapatry.","authors":"Richard M Sibly, Robert N Curnow","doi":"10.1093/jeb/voae160","DOIUrl":"https://doi.org/10.1093/jeb/voae160","url":null,"abstract":"<p><p>The time needed for the evolution of mating cues that distinguish species, such as species-specific songs or plumage coloration in birds, has received little attention. Aiming to gain some understanding of the timing of the evolutionary process we here present models of how mating cues evolve in populations split into subpopulations between which there may (parapatry) or may not (allopatry) be migration. Mating cues can be either neutral or directly selected. In models in which evolution commences with a substitution at a neutral mating-cue locus, under allopatry there is no selection on the mating cue, but under parapatry selection may be induced on the mating cue by the selective conditions in the subpopulations and the migration rates between them. We use simulation to calculate how selection pressures on mating cues then depend on selective conditions in subpopulations and migration rates between them. In the second part of the paper we demonstrate quantitatively how the resulting selection pressures on new mating cues together with mutation rate affect speciation time. Our results suggest that species-specific songs or plumage colorations that are selectively neutral evolve faster under parapatry than under allopatry, and this may explain the short speciation times that are sometimes reported. Although our modelling assumptions are restrictive so that caution is needed in comparing the results to empirical data, we hope that our main results, showing quantitatively how parapatry can reduce speciation times, will encourage further work relaxing model assumptions or studying different models of mate choice.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2024-12-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142958132","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Alex H Waugh, Michael A Catto, Samuel V Arsenault, Sasha Kay, Kenneth G Ross, Brendan G Hunt
Characterizing molecular underpinnings of plastic traits and balanced polymorphisms represent two important goals of evolutionary biology. Fire ant gynes (pre-reproductive queens) provide an ideal system to study potential links between these phenomena because they exhibit both supergene-mediated polymorphism and nutritional plasticity in weight and colony-founding behavior. Gynes with the inversion supergene haplotype are lightweight and depend on existing workers to initiate reproduction. Gynes with only the ancestral, non-inverted gene arrangement accumulate more nutrient reserves as adults and, in a distinct colony-founding behavior, initiate reproduction without help from workers. However, when such gynes overwinter in the natal nest they develop an environmentally induced lightweight phenotype and colony-founding behavior, similar to gynes with the inversion haplotype that have not overwintered. To evaluate the extent of shared mechanisms between plasticity and balanced polymorphism in fire ant gyne traits, we assessed whether genes with expression variation linked to overwintering plasticity may be affected by evolutionary divergence between supergene haplotypes. To do so, we first compared transcriptional profiles of brains and ovaries from overwintered and non-overwintered gynes to identify plasticity-associated genes. These genes were enriched for metabolic and behavioral functions. Next, we compared plasticity-associated genes to those differentially expressed by supergene genotype, revealing a significant overlap of the two sets in ovarian tissues. We also identified sequence substitutions between supergene variants of multiple plasticity-associated genes, consistent with a scenario in which an ancestrally plastic phenotype responsive to an environmental condition became increasingly genetically regulated.
{"title":"Molecular underpinnings of plasticity and supergene-mediated polymorphism in fire ant queens.","authors":"Alex H Waugh, Michael A Catto, Samuel V Arsenault, Sasha Kay, Kenneth G Ross, Brendan G Hunt","doi":"10.1093/jeb/voae159","DOIUrl":"https://doi.org/10.1093/jeb/voae159","url":null,"abstract":"<p><p>Characterizing molecular underpinnings of plastic traits and balanced polymorphisms represent two important goals of evolutionary biology. Fire ant gynes (pre-reproductive queens) provide an ideal system to study potential links between these phenomena because they exhibit both supergene-mediated polymorphism and nutritional plasticity in weight and colony-founding behavior. Gynes with the inversion supergene haplotype are lightweight and depend on existing workers to initiate reproduction. Gynes with only the ancestral, non-inverted gene arrangement accumulate more nutrient reserves as adults and, in a distinct colony-founding behavior, initiate reproduction without help from workers. However, when such gynes overwinter in the natal nest they develop an environmentally induced lightweight phenotype and colony-founding behavior, similar to gynes with the inversion haplotype that have not overwintered. To evaluate the extent of shared mechanisms between plasticity and balanced polymorphism in fire ant gyne traits, we assessed whether genes with expression variation linked to overwintering plasticity may be affected by evolutionary divergence between supergene haplotypes. To do so, we first compared transcriptional profiles of brains and ovaries from overwintered and non-overwintered gynes to identify plasticity-associated genes. These genes were enriched for metabolic and behavioral functions. Next, we compared plasticity-associated genes to those differentially expressed by supergene genotype, revealing a significant overlap of the two sets in ovarian tissues. We also identified sequence substitutions between supergene variants of multiple plasticity-associated genes, consistent with a scenario in which an ancestrally plastic phenotype responsive to an environmental condition became increasingly genetically regulated.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2024-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142856578","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
In eutherians, one of the X chromosomes in each cell of the early female embryo is rendered transcriptionally silent through X chromosome inactivation. The choice of which X chromosome to inactivate takes place independently in each cell and is stably inherited through development, leading to a roughly 50:50 ratio of cells in the adult body expressing one or the other X chromosome. However, X chromosome inactivation can be skewed, with certain X chromosomes showing a heritable tendency to avoid inactivation. Using population genetic models, we test whether genetic variation for this trait can be maintained by linked sexually antagonistic selection. In favor of this hypothesis, we find that a neutral modifier that affects the chances of its chromosome's inactivation-e.g., a variant of the X controlling element (Xce)-can spread when linked to a sexually antagonistic gene. We explore the logic of this modifier's spread, which we find to be similar in many respects to that of a modifier of dominance. We also test for the presence of a "drift barrier"-i.e., a population size below which the indirect selective force favoring the modifier becomes too weak to overcome drift. On balance, we find that sexual antagonism may encourage the spread of skewed X chromosome inactivation, but only under favorable conditions.
{"title":"Skewed X Chromosome Inactivation As A Response To Sexually Antagonistic Selection.","authors":"Naomi L Greenberg, Manus M Patten","doi":"10.1093/jeb/voae157","DOIUrl":"https://doi.org/10.1093/jeb/voae157","url":null,"abstract":"<p><p>In eutherians, one of the X chromosomes in each cell of the early female embryo is rendered transcriptionally silent through X chromosome inactivation. The choice of which X chromosome to inactivate takes place independently in each cell and is stably inherited through development, leading to a roughly 50:50 ratio of cells in the adult body expressing one or the other X chromosome. However, X chromosome inactivation can be skewed, with certain X chromosomes showing a heritable tendency to avoid inactivation. Using population genetic models, we test whether genetic variation for this trait can be maintained by linked sexually antagonistic selection. In favor of this hypothesis, we find that a neutral modifier that affects the chances of its chromosome's inactivation-e.g., a variant of the X controlling element (Xce)-can spread when linked to a sexually antagonistic gene. We explore the logic of this modifier's spread, which we find to be similar in many respects to that of a modifier of dominance. We also test for the presence of a \"drift barrier\"-i.e., a population size below which the indirect selective force favoring the modifier becomes too weak to overcome drift. On balance, we find that sexual antagonism may encourage the spread of skewed X chromosome inactivation, but only under favorable conditions.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142830749","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Recombination diversifies the genomes of offspring, influences the evolutionary dynamics of populations, and ensures that chromosomes segregate properly during meiosis. Individuals recombine at different rates but observed levels of variation in recombination rate remain mostly unexplained. Genetic dissection of differences in recombination rate within and between species provides a powerful framework for understanding how this trait evolves. In this Perspective, I amalgamate published findings from genetic studies of variation in the genome-wide number of crossovers within and between species, and I use exploratory analyses to identify preliminary patterns. The narrow-sense heritability of crossover count is consistently low, indicating limited resemblance among relatives and predicting a weak response to short-term selection. Variants associated with crossover number within populations span the range of minor allele frequency. The size of the additive effect of recombination-associated variants, along with a negative correlation between this effect and minor allele frequency, raises the prospect that mutations inducing phenotypic shifts larger than a few crossovers are deleterious, though the contributions of methodological biases to these patterns deserve investigation. Quantitative trait loci that contribute to differences between populations or species alter crossover number in both directions, a pattern inconsistent with selection toward a constant optimum for this trait. Building on this characterization of genetic variation in crossover number within and between species, I describe fruitful avenues for future research. Better integrating recombination rate into quantitative genetics will reveal the balance of evolutionary forces responsible for genetic variation in this trait that shapes inheritance.
{"title":"Genetics of Recombination Rate Variation Within and Between Species.","authors":"Bret A Payseur","doi":"10.1093/jeb/voae158","DOIUrl":"10.1093/jeb/voae158","url":null,"abstract":"<p><p>Recombination diversifies the genomes of offspring, influences the evolutionary dynamics of populations, and ensures that chromosomes segregate properly during meiosis. Individuals recombine at different rates but observed levels of variation in recombination rate remain mostly unexplained. Genetic dissection of differences in recombination rate within and between species provides a powerful framework for understanding how this trait evolves. In this Perspective, I amalgamate published findings from genetic studies of variation in the genome-wide number of crossovers within and between species, and I use exploratory analyses to identify preliminary patterns. The narrow-sense heritability of crossover count is consistently low, indicating limited resemblance among relatives and predicting a weak response to short-term selection. Variants associated with crossover number within populations span the range of minor allele frequency. The size of the additive effect of recombination-associated variants, along with a negative correlation between this effect and minor allele frequency, raises the prospect that mutations inducing phenotypic shifts larger than a few crossovers are deleterious, though the contributions of methodological biases to these patterns deserve investigation. Quantitative trait loci that contribute to differences between populations or species alter crossover number in both directions, a pattern inconsistent with selection toward a constant optimum for this trait. Building on this characterization of genetic variation in crossover number within and between species, I describe fruitful avenues for future research. Better integrating recombination rate into quantitative genetics will reveal the balance of evolutionary forces responsible for genetic variation in this trait that shapes inheritance.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142830748","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Audrey Tremblay, Fanie Pelletier, Andrew Macdonald, Dany Garant
Several studies have emphasized that phenotypic plasticity should be a key mechanism to cope with current rapid environmental changes by allowing individuals to quickly express new adaptive phenotypes. Yet, few studies have investigated the evolutionary potential of plasticity for multiple traits simultaneously and using several different environmental variables. Here, we assess the extent of variation in, and the selection acting on phenotypic plasticity of key ecological traits, laying date and clutch size, using five environmental variables, in a Tree swallow (Tachycineta bicolor) population monitored since 2004. While we found some variation among females in their mean laying date and plasticity, we found evidence of selection acting only on mean laying date. We found no variation among females in mean clutch size or plasticity, such that we could not assess selection acting on either. Our results suggest that the evolutionary potential of plasticity in the population under study is limited, especially for clutch size. More studies investigating plasticity in wild populations and incorporating multiple traits and environmental variables are needed to understand future responses of animal populations to environmental changes.
{"title":"Individual variation and selection for phenotypic plasticity of laying date and clutch size across different environmental conditions in Tree swallow (Tachycineta bicolor).","authors":"Audrey Tremblay, Fanie Pelletier, Andrew Macdonald, Dany Garant","doi":"10.1093/jeb/voae156","DOIUrl":"https://doi.org/10.1093/jeb/voae156","url":null,"abstract":"<p><p>Several studies have emphasized that phenotypic plasticity should be a key mechanism to cope with current rapid environmental changes by allowing individuals to quickly express new adaptive phenotypes. Yet, few studies have investigated the evolutionary potential of plasticity for multiple traits simultaneously and using several different environmental variables. Here, we assess the extent of variation in, and the selection acting on phenotypic plasticity of key ecological traits, laying date and clutch size, using five environmental variables, in a Tree swallow (Tachycineta bicolor) population monitored since 2004. While we found some variation among females in their mean laying date and plasticity, we found evidence of selection acting only on mean laying date. We found no variation among females in mean clutch size or plasticity, such that we could not assess selection acting on either. Our results suggest that the evolutionary potential of plasticity in the population under study is limited, especially for clutch size. More studies investigating plasticity in wild populations and incorporating multiple traits and environmental variables are needed to understand future responses of animal populations to environmental changes.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2024-12-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142824670","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Peter Nabutanyi, Alitha Edison, Peter Czuppon, Shuqing Xu, Meike Wittmann
Individuals living in heterogeneous environments often choose microenvironments that provide benefits to their fitness. Theory predicts that such niche choice can promote rapid adaptation to novel environments and help maintain genetic diversity. An open question of large applied importance is how niche choice and niche choice evolution affect the evolution of insecticide resistance in phytophagous insects. We, therefore, developed an individual-based model based on phytophagous insects to examine the evolution of insecticide resistance and niche choice via oviposition preferences. To find biologically realistic parameter ranges, we performed an empirical literature survey on insecticide resistance in major agricultural pests and also conducted a density-dependent survival experiment using potato beetles. We find that, in comparison to a scenario where individuals randomly oviposit eggs on toxic or non-toxic plants, the evolution of niche choice generally leads to slower evolution of resistance and facilitates the coexistence of different phenotypes. Our simulations also reveal that recombination rate and dominance effects can influence the evolution of both niche choice and resistance. Thus, this study provides new insights into the effects of niche choice on resistance evolution and highlights the need for more studies on the genetic basis of resistance and choice.
{"title":"The role of evolving niche choice in herbivore adaptation to host plants.","authors":"Peter Nabutanyi, Alitha Edison, Peter Czuppon, Shuqing Xu, Meike Wittmann","doi":"10.1093/jeb/voae154","DOIUrl":"https://doi.org/10.1093/jeb/voae154","url":null,"abstract":"<p><p>Individuals living in heterogeneous environments often choose microenvironments that provide benefits to their fitness. Theory predicts that such niche choice can promote rapid adaptation to novel environments and help maintain genetic diversity. An open question of large applied importance is how niche choice and niche choice evolution affect the evolution of insecticide resistance in phytophagous insects. We, therefore, developed an individual-based model based on phytophagous insects to examine the evolution of insecticide resistance and niche choice via oviposition preferences. To find biologically realistic parameter ranges, we performed an empirical literature survey on insecticide resistance in major agricultural pests and also conducted a density-dependent survival experiment using potato beetles. We find that, in comparison to a scenario where individuals randomly oviposit eggs on toxic or non-toxic plants, the evolution of niche choice generally leads to slower evolution of resistance and facilitates the coexistence of different phenotypes. Our simulations also reveal that recombination rate and dominance effects can influence the evolution of both niche choice and resistance. Thus, this study provides new insights into the effects of niche choice on resistance evolution and highlights the need for more studies on the genetic basis of resistance and choice.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2024-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142814820","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Graham A McCulloch, Brodie J Foster, Gracie C Kroos, Yasmin Foster, Steven Ni, Marianne F S Vogel, Jonathan M Waters
Wing reduction is a common feature of upland insect communities. This phenomenon is thought to be primarily driven by selection against flight, which is typically unfavorable in upland environments due to high winds and cold temperatures. In some insect taxa, wing-reduction has been directly linked to increased fecundity. However, few studies have directly tested for shifts in fecundity linked to flight musculature. Here we test for dispersal-fecundity trade-offs in the widespread subalpine stonefly Zelandoperla fenestrata. Our analysis of 450 stoneflies across 81 localities reveals significant dispersal-fecundity tradeoffs. Specifically, we identify a positive association between the size of their flight muscles and the length of their wings, and a negative association between wing length and ovarian mass. Furthermore, we found a significant negative relationship between flight musculature and ovary mass. These results represent a rare example of a dispersal-fecundity tradeoff in the wild, and illustrate that such tradeoffs can potentially involve corresponding reductions in both flight musculature and wing development. Our findings suggest that widespread taxa subject to variable environmental conditions may benefit from flexible allocation of energetic resources.
{"title":"Dispersal-fecundity trade-offs in wild insect populations.","authors":"Graham A McCulloch, Brodie J Foster, Gracie C Kroos, Yasmin Foster, Steven Ni, Marianne F S Vogel, Jonathan M Waters","doi":"10.1093/jeb/voae155","DOIUrl":"https://doi.org/10.1093/jeb/voae155","url":null,"abstract":"<p><p>Wing reduction is a common feature of upland insect communities. This phenomenon is thought to be primarily driven by selection against flight, which is typically unfavorable in upland environments due to high winds and cold temperatures. In some insect taxa, wing-reduction has been directly linked to increased fecundity. However, few studies have directly tested for shifts in fecundity linked to flight musculature. Here we test for dispersal-fecundity trade-offs in the widespread subalpine stonefly Zelandoperla fenestrata. Our analysis of 450 stoneflies across 81 localities reveals significant dispersal-fecundity tradeoffs. Specifically, we identify a positive association between the size of their flight muscles and the length of their wings, and a negative association between wing length and ovarian mass. Furthermore, we found a significant negative relationship between flight musculature and ovary mass. These results represent a rare example of a dispersal-fecundity tradeoff in the wild, and illustrate that such tradeoffs can potentially involve corresponding reductions in both flight musculature and wing development. Our findings suggest that widespread taxa subject to variable environmental conditions may benefit from flexible allocation of energetic resources.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2024-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142814819","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Masahito Tsuboi, Jacqueline Sztepanacz, Stephen De Lisle, Kjetil L Voje, Mark Grabowski, Melanie J Hopkins, Arthur Porto, Meghan Balk, Mikael Pontarp, Daniela Rossoni, Laura S Hildesheim, Quentin J-B Horta-Lacueva, Niklas Hohmann, Agnes Holstad, Moritz Lürig, Lisandro Milocco, Sofie Nilén, Arianna Passarotto, Erik I Svensson, Cristina Villegas, Erica Winslott, Lee Hsiang Liow, Gene Hunt, Alan C Love, David Houle
The relationship between the evolutionary dynamics observed in contemporary populations (microevolution) and evolution on timescales of millions of years (macroevolution) has been a topic of considerable debate. Historically, this debate centers on inconsistencies between microevolutionary processes and macroevolutionary patterns. Here, we characterize a striking exception: emerging evidence indicates that standing variation in contemporary populations and macroevolutionary rates of phenotypic divergence is often positively correlated. This apparent consistency between micro- and macroevolution is paradoxical because it contradicts our previous understanding of phenotypic evolution and is so far unexplained. Here, we explore the prospects for bridging evolutionary timescales through an examination of this "paradox of predictability." We begin by explaining why the divergence-variance correlation is a paradox, followed by data analysis to show that the correlation is a general phenomenon across a broad range of temporal scales, from a few generations to tens of millions of years. Then we review complementary approaches from quantitative genetics, comparative morphology, evo-devo, and paleontology to argue that they can help to address the paradox from the shared vantage point of recent work on evolvability. In conclusion, we recommend a methodological orientation that combines different kinds of short-term and long-term data using multiple analytical frameworks in an interdisciplinary research program. Such a program will increase our general understanding of how evolution works within and across timescales.
{"title":"The paradox of predictability provides a bridge between micro- and macroevolution.","authors":"Masahito Tsuboi, Jacqueline Sztepanacz, Stephen De Lisle, Kjetil L Voje, Mark Grabowski, Melanie J Hopkins, Arthur Porto, Meghan Balk, Mikael Pontarp, Daniela Rossoni, Laura S Hildesheim, Quentin J-B Horta-Lacueva, Niklas Hohmann, Agnes Holstad, Moritz Lürig, Lisandro Milocco, Sofie Nilén, Arianna Passarotto, Erik I Svensson, Cristina Villegas, Erica Winslott, Lee Hsiang Liow, Gene Hunt, Alan C Love, David Houle","doi":"10.1093/jeb/voae103","DOIUrl":"10.1093/jeb/voae103","url":null,"abstract":"<p><p>The relationship between the evolutionary dynamics observed in contemporary populations (microevolution) and evolution on timescales of millions of years (macroevolution) has been a topic of considerable debate. Historically, this debate centers on inconsistencies between microevolutionary processes and macroevolutionary patterns. Here, we characterize a striking exception: emerging evidence indicates that standing variation in contemporary populations and macroevolutionary rates of phenotypic divergence is often positively correlated. This apparent consistency between micro- and macroevolution is paradoxical because it contradicts our previous understanding of phenotypic evolution and is so far unexplained. Here, we explore the prospects for bridging evolutionary timescales through an examination of this \"paradox of predictability.\" We begin by explaining why the divergence-variance correlation is a paradox, followed by data analysis to show that the correlation is a general phenomenon across a broad range of temporal scales, from a few generations to tens of millions of years. Then we review complementary approaches from quantitative genetics, comparative morphology, evo-devo, and paleontology to argue that they can help to address the paradox from the shared vantage point of recent work on evolvability. In conclusion, we recommend a methodological orientation that combines different kinds of short-term and long-term data using multiple analytical frameworks in an interdisciplinary research program. Such a program will increase our general understanding of how evolution works within and across timescales.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"1413-1432"},"PeriodicalIF":2.1,"publicationDate":"2024-12-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142114322","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
To quantify selection acting on a trait, methods have been developed using either within or between-species variation. However, methods using within-species variation do not integrate the changes at the macro-evolutionary scale. Conversely, current methods using between-species variation usually discard within-species variation, thus not accounting for processes at the micro-evolutionary scale. The main goal of this study is to define a neutrality index for a quantitative trait, by combining within- and between-species variation. This neutrality index integrates nucleotide polymorphism and divergence for normalizing trait variation. As such, it does not require estimation of population size nor of time of speciation for normalization. Our index can be used to seek deviation from the null model of neutral evolution, and test for diversifying selection. Applied to brain mass and body mass at the mammalian scale, we show that brain mass is under diversifying selection. Finally, we show that our test is not sensitive to the assumption that population sizes, mutation rates and generation time are constant across the phylogeny, and automatically adjust for it.
{"title":"Detecting diversifying selection for a trait from within and between-species genotypes and phenotypes.","authors":"T Latrille, M Bastian, T Gaboriau, N Salamin","doi":"10.1093/jeb/voae084","DOIUrl":"10.1093/jeb/voae084","url":null,"abstract":"<p><p>To quantify selection acting on a trait, methods have been developed using either within or between-species variation. However, methods using within-species variation do not integrate the changes at the macro-evolutionary scale. Conversely, current methods using between-species variation usually discard within-species variation, thus not accounting for processes at the micro-evolutionary scale. The main goal of this study is to define a neutrality index for a quantitative trait, by combining within- and between-species variation. This neutrality index integrates nucleotide polymorphism and divergence for normalizing trait variation. As such, it does not require estimation of population size nor of time of speciation for normalization. Our index can be used to seek deviation from the null model of neutral evolution, and test for diversifying selection. Applied to brain mass and body mass at the mammalian scale, we show that brain mass is under diversifying selection. Finally, we show that our test is not sensitive to the assumption that population sizes, mutation rates and generation time are constant across the phylogeny, and automatically adjust for it.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"1538-1550"},"PeriodicalIF":2.1,"publicationDate":"2024-12-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141591936","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Coevolution can occur because of species interactions. However, it remains unclear how coevolutionary processes translate into the accumulation of species richness over macroevolutionary timescales. Assuming speciation occurs as a result of genetic differentiation across space due to dispersal limitation, we examine the effects of coevolution-induced phenotypic selection on species diversification. Based on the idea that dispersers often carry novel phenotypes, we propose and test two hypotheses. (1) Stability hypothesis: selection against phenotypic novelty enhances species diversification by strengthening dispersal limitation. (2) Novelty hypothesis: selection for phenotypic novelty impedes species diversification by weakening dispersal limitation. We simulate clade co-diversification using an individual-based model, considering scenarios where phenotypic selection is shaped by neutral dynamics, mutualistic coevolution, or antagonistic coevolution, where coevolution operates through trait matching or trait difference, and where the strength of coevolutionary selection is symmetrical or asymmetrical. Our key assumption that interactions occur between an independent party (whose individuals can establish or persist independently, e.g., hosts) and a dependent party (whose individuals cannot establish or persist independently, for example, parasites or obligate mutualists) yields two contrasting results. The stability hypothesis is supported in the dependent clade but not in the independent clade. Conversely, the novelty hypothesis is supported in the independent clade but not in the dependent clade. These results are partially corroborated by empirical dispersal data, suggesting that these mechanisms might potentially explain the diversification of some of the most species-rich clades in the Tree of Life.
{"title":"Coevolution-induced selection for and against phenotypic novelty shapes species richness in clade co-diversification.","authors":"Yichao Zeng, David H Hembry","doi":"10.1093/jeb/voae069","DOIUrl":"10.1093/jeb/voae069","url":null,"abstract":"<p><p>Coevolution can occur because of species interactions. However, it remains unclear how coevolutionary processes translate into the accumulation of species richness over macroevolutionary timescales. Assuming speciation occurs as a result of genetic differentiation across space due to dispersal limitation, we examine the effects of coevolution-induced phenotypic selection on species diversification. Based on the idea that dispersers often carry novel phenotypes, we propose and test two hypotheses. (1) Stability hypothesis: selection against phenotypic novelty enhances species diversification by strengthening dispersal limitation. (2) Novelty hypothesis: selection for phenotypic novelty impedes species diversification by weakening dispersal limitation. We simulate clade co-diversification using an individual-based model, considering scenarios where phenotypic selection is shaped by neutral dynamics, mutualistic coevolution, or antagonistic coevolution, where coevolution operates through trait matching or trait difference, and where the strength of coevolutionary selection is symmetrical or asymmetrical. Our key assumption that interactions occur between an independent party (whose individuals can establish or persist independently, e.g., hosts) and a dependent party (whose individuals cannot establish or persist independently, for example, parasites or obligate mutualists) yields two contrasting results. The stability hypothesis is supported in the dependent clade but not in the independent clade. Conversely, the novelty hypothesis is supported in the independent clade but not in the dependent clade. These results are partially corroborated by empirical dispersal data, suggesting that these mechanisms might potentially explain the diversification of some of the most species-rich clades in the Tree of Life.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"1510-1522"},"PeriodicalIF":2.1,"publicationDate":"2024-12-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141187025","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}