Mitochondrial paraphyly between arthropod species is not uncommon and has been speculated to largely be the result of incomplete lineage sorting (ILS) of ancestral variation within the common ancestor of both species, with hybridization playing only a minor role. However, in the absence of comparable nuclear genetic data, the relative roles of ILS and hybridization in explaining mitochondrial DNA (mtDNA) paraphyly remain unclear. Hybridization itself is a multifaceted gateway to mtDNA paraphyly, which may lead to paraphyly across both the nuclear and mitochondrial genomes, or paraphyly that is largely restricted to the mitochondrial genome. These different outcomes will depend upon the frequency of hybridization, its demographic context, and the extent to which mtDNA is subject to direct selection, indirect selection, or neutral processes. Here, we describe extensive mtDNA paraphyly between two species of iron-clad beetle (Zopheridae) and evaluate competing explanations for its origin. We first test between hypotheses of ILS and hybridization, revealing strong nuclear genetic differentiation between species, but with the complete replacement of Tarphius simplex mtDNA through the introgression of at least 5 mtDNA haplotypes from T. canariensis. We then contrast explanations of direct selection, indirect selection, or genetic drift for observed patterns of mtDNA introgression. Our results highlight how introgression can lead to complex patterns of mtDNA paraphyly across arthropod species, while simultaneously revealing the challenges for understanding the selective or neutral drivers that underpin such patterns.
{"title":"Arthropod mtDNA paraphyly: a case study of introgressive origin.","authors":"Víctor Noguerales, Brent C Emerson","doi":"10.1093/jeb/voae152","DOIUrl":"10.1093/jeb/voae152","url":null,"abstract":"<p><p>Mitochondrial paraphyly between arthropod species is not uncommon and has been speculated to largely be the result of incomplete lineage sorting (ILS) of ancestral variation within the common ancestor of both species, with hybridization playing only a minor role. However, in the absence of comparable nuclear genetic data, the relative roles of ILS and hybridization in explaining mitochondrial DNA (mtDNA) paraphyly remain unclear. Hybridization itself is a multifaceted gateway to mtDNA paraphyly, which may lead to paraphyly across both the nuclear and mitochondrial genomes, or paraphyly that is largely restricted to the mitochondrial genome. These different outcomes will depend upon the frequency of hybridization, its demographic context, and the extent to which mtDNA is subject to direct selection, indirect selection, or neutral processes. Here, we describe extensive mtDNA paraphyly between two species of iron-clad beetle (Zopheridae) and evaluate competing explanations for its origin. We first test between hypotheses of ILS and hybridization, revealing strong nuclear genetic differentiation between species, but with the complete replacement of Tarphius simplex mtDNA through the introgression of at least 5 mtDNA haplotypes from T. canariensis. We then contrast explanations of direct selection, indirect selection, or genetic drift for observed patterns of mtDNA introgression. Our results highlight how introgression can lead to complex patterns of mtDNA paraphyly across arthropod species, while simultaneously revealing the challenges for understanding the selective or neutral drivers that underpin such patterns.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"272-283"},"PeriodicalIF":2.1,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142808395","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}
Camille E Wendlandt, Julio Avelar-Barragan, Avissa J Zomorrodian, Khadija Al-Moussawi, Stephanie S Porter, Joel L Sachs
Plant hosts can gain significant growth benefits from symbiosis with microbes, but these benefits could be threatened by divergent fitness interests among partners. Here, we measured fitness outcomes in symbiosis, by varying the genotypes of both microbes and hosts, to examine scenarios that might favour uncooperative symbionts. We studied associations between Acmispon strigosus, an annual legume native to California, and its nitrogen-fixing symbionts in the genus Bradyrhizobium. Bradyrhizobium symbionts form root nodules on compatible hosts, with strains varying from effective, fixing substantial nitrogen for the host, to ineffective strains that do not fix nitrogen and provide no benefit to host growth. We co-inoculated four A. strigosus plant lines with nine combinations of effective and ineffective Bradyrhizobium strains and measured the relative fitness of ineffective strains within individual nodules, as hosts must select against uncooperative symbionts to maintain benefits. In mixed infections, ineffective strains always had lower relative fitness in nodules compared to beneficial strains, consistent with efficient punishment of non-fixing rhizobia. However, ineffective strains exhibited genotypic variation in their fitness in nodules within individual nodules co-infected with a beneficial strain, suggesting a role for symbiont competitiveness in shaping this joint phenotype. Variation in symbiont fitness during co-inoculations did not measurably affect plant performance, suggesting that predicted conflict over the joint phenotype of rhizobia fitness has negligible effect on the host.
{"title":"Host control by Acmispon strigosus constrains fitness gains of ineffective Bradyrhizobium symbionts in mixed infections.","authors":"Camille E Wendlandt, Julio Avelar-Barragan, Avissa J Zomorrodian, Khadija Al-Moussawi, Stephanie S Porter, Joel L Sachs","doi":"10.1093/jeb/voae151","DOIUrl":"10.1093/jeb/voae151","url":null,"abstract":"<p><p>Plant hosts can gain significant growth benefits from symbiosis with microbes, but these benefits could be threatened by divergent fitness interests among partners. Here, we measured fitness outcomes in symbiosis, by varying the genotypes of both microbes and hosts, to examine scenarios that might favour uncooperative symbionts. We studied associations between Acmispon strigosus, an annual legume native to California, and its nitrogen-fixing symbionts in the genus Bradyrhizobium. Bradyrhizobium symbionts form root nodules on compatible hosts, with strains varying from effective, fixing substantial nitrogen for the host, to ineffective strains that do not fix nitrogen and provide no benefit to host growth. We co-inoculated four A. strigosus plant lines with nine combinations of effective and ineffective Bradyrhizobium strains and measured the relative fitness of ineffective strains within individual nodules, as hosts must select against uncooperative symbionts to maintain benefits. In mixed infections, ineffective strains always had lower relative fitness in nodules compared to beneficial strains, consistent with efficient punishment of non-fixing rhizobia. However, ineffective strains exhibited genotypic variation in their fitness in nodules within individual nodules co-infected with a beneficial strain, suggesting a role for symbiont competitiveness in shaping this joint phenotype. Variation in symbiont fitness during co-inoculations did not measurably affect plant performance, suggesting that predicted conflict over the joint phenotype of rhizobia fitness has negligible effect on the host.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"261-271"},"PeriodicalIF":2.1,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142808397","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}
Sam Edwards, Andreas Naundrup, Paul G Becher, Henrik H De Fine Licht
Host-pathogen infections and possible effects on co-evolutionary patterns depend on the genotypes of both host and pathogen. Obligate fungal pathogens of plants are often characterized by host-pathogen genotype-by-genotype (GxG) interactions, but whether these patterns exist in obligate insect fungal pathogens is unclear. We take advantage of the obligate insect pathogenic fungus Entomophthora muscae, where individual isolates are specific to different dipteran host species in nature but can cross-infect multiple fly species in the laboratory. We collected three new isolates of E. muscae from Drosophila species. Phylogenetic analysis showed that Drosophila-isolated E. muscae represents a distinct geographically widespread Drosophila lineage compared to the house fly (Musca domestica) or Delia species-isolated E. muscae. We used the three new E. muscae isolates from Drosophila spp. together with a genetically distinct E. muscae isolate from house flies and assessed their virulence in a cross-infection experiment using one house fly, three Drosophila suzukii, and two D. melanogaster genotypes as hosts. All fungal isolates successfully infected hosts, induced behavioural manipulation, sporulated in all fly hosts, and differed in virulence between host genotypes, revealing GxG interactions. While house flies were most susceptible to fungal infection with 99% mortality, we found a lower virulence of 49% and 25% mortality in D. melanogaster and D. suzukii genotypes, respectively. Furthermore, all isolates harboured a specific mycovirus (family Iflaviridae), but co-phylogenetic branching patterns did not support fungus-virus co-speciation. We show that the genetic makeup of both fungal pathogen and fly host influence E. muscae infectivity, confirming GxG interactions in obligate fly fungal pathogens.
{"title":"Patterns of genotype-specific interactions in an obligate host-specific insect pathogenic fungus.","authors":"Sam Edwards, Andreas Naundrup, Paul G Becher, Henrik H De Fine Licht","doi":"10.1093/jeb/voae149","DOIUrl":"10.1093/jeb/voae149","url":null,"abstract":"<p><p>Host-pathogen infections and possible effects on co-evolutionary patterns depend on the genotypes of both host and pathogen. Obligate fungal pathogens of plants are often characterized by host-pathogen genotype-by-genotype (GxG) interactions, but whether these patterns exist in obligate insect fungal pathogens is unclear. We take advantage of the obligate insect pathogenic fungus Entomophthora muscae, where individual isolates are specific to different dipteran host species in nature but can cross-infect multiple fly species in the laboratory. We collected three new isolates of E. muscae from Drosophila species. Phylogenetic analysis showed that Drosophila-isolated E. muscae represents a distinct geographically widespread Drosophila lineage compared to the house fly (Musca domestica) or Delia species-isolated E. muscae. We used the three new E. muscae isolates from Drosophila spp. together with a genetically distinct E. muscae isolate from house flies and assessed their virulence in a cross-infection experiment using one house fly, three Drosophila suzukii, and two D. melanogaster genotypes as hosts. All fungal isolates successfully infected hosts, induced behavioural manipulation, sporulated in all fly hosts, and differed in virulence between host genotypes, revealing GxG interactions. While house flies were most susceptible to fungal infection with 99% mortality, we found a lower virulence of 49% and 25% mortality in D. melanogaster and D. suzukii genotypes, respectively. Furthermore, all isolates harboured a specific mycovirus (family Iflaviridae), but co-phylogenetic branching patterns did not support fungus-virus co-speciation. We show that the genetic makeup of both fungal pathogen and fly host influence E. muscae infectivity, confirming GxG interactions in obligate fly fungal pathogens.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"225-239"},"PeriodicalIF":2.1,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142822837","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}
The force of selection describes the sensitivity of population growth to changes in life history parameters, with a focus usually on the survival probabilities from one age class to the next. Importantly, according to Hamilton the force of selection generally decreases after the onset of reproduction, thereby providing a possible explanation for patterns of senescence. A second characteristic feature is that the force of selection remains constant up to the age of first reproduction. This latter observation, however, rests on the assumption that offspring become independent from their parents right after birth. I show here in a minimal model that if offspring are fully reliant on their parents, either during early embryonal development or via parental care at later stages, and during this time prevent their parents from entering a new bout of reproduction, the force of selection on offspring survival generally increases up until the age at which offspring become independent. This provides a possible explanation for the commonly observed pattern of decreasing mortality during early ontogeny. Furthermore, genes acting during recurrent life stages are observed to experience a heightened force of selection compared with genes that act strictly age specifically, demonstrating the need to develop a mechanistic understanding of gene activation patterns through which to consider life history evolution.
{"title":"Effects of development and parental care on Hamilton's force of selection.","authors":"Christoph Netz","doi":"10.1093/jeb/voae131","DOIUrl":"10.1093/jeb/voae131","url":null,"abstract":"<p><p>The force of selection describes the sensitivity of population growth to changes in life history parameters, with a focus usually on the survival probabilities from one age class to the next. Importantly, according to Hamilton the force of selection generally decreases after the onset of reproduction, thereby providing a possible explanation for patterns of senescence. A second characteristic feature is that the force of selection remains constant up to the age of first reproduction. This latter observation, however, rests on the assumption that offspring become independent from their parents right after birth. I show here in a minimal model that if offspring are fully reliant on their parents, either during early embryonal development or via parental care at later stages, and during this time prevent their parents from entering a new bout of reproduction, the force of selection on offspring survival generally increases up until the age at which offspring become independent. This provides a possible explanation for the commonly observed pattern of decreasing mortality during early ontogeny. Furthermore, genes acting during recurrent life stages are observed to experience a heightened force of selection compared with genes that act strictly age specifically, demonstrating the need to develop a mechanistic understanding of gene activation patterns through which to consider life history evolution.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"63-69"},"PeriodicalIF":2.1,"publicationDate":"2025-01-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142512151","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}
Dispersal is a key demographic parameter that plays an important role in determining spatial population dynamics and genetic structure. Linking differences in dispersal patterns to life-history traits is often confounded by inconsistent environmental pressures experienced by different populations. To explore the relationship between dispersal and life history, we focus on a site where oviparous and viviparous lineages of the common lizard (Zootoca vivipara) are found adjacent to each other. We take advantage of this shared environment to investigate parity-specific dispersal patterns using high-resolution, individual-level spatial-genetic autocorrelation and population genomic approaches (11,726 single nucleotide polymorphisms; 293 oviparous and 310 viviparous individuals). We found isolation-by-distance patterns to be present in both the oviparous and viviparous populations. Density was 2.5 times higher in the oviparous population than the viviparous one, though heterozygosity and genetic diversity measures were similar in the two populations. We found marked differences in the extent of genetic neighbourhoods between the lineages, with the viviparous population showing both dispersal (σ) and spatial-genetic autocorrelation (Moran's I) at 2-fold greater geographic distances than the oviparous population. We found clear evidence of male-biased dispersal from genetic estimates in the viviparous population. In the oviparous population, evidence of male-biased dispersal was weak or absent. These differences are likely to be closely linked to specific requirements of the alternative reproductive strategies and may be the demographic consequences of mother-offspring interactions. Fine-scale geographic and individual-level measures are essential to understanding parity mode differences at microevolutionary scales and to better identifying their ecological and evolutionary impacts.
{"title":"Parity-specific differences in spatial genetics and dispersal in the common lizard.","authors":"Darren C Hunter, Jean Clobert, Kathryn R Elmer","doi":"10.1093/jeb/voae133","DOIUrl":"10.1093/jeb/voae133","url":null,"abstract":"<p><p>Dispersal is a key demographic parameter that plays an important role in determining spatial population dynamics and genetic structure. Linking differences in dispersal patterns to life-history traits is often confounded by inconsistent environmental pressures experienced by different populations. To explore the relationship between dispersal and life history, we focus on a site where oviparous and viviparous lineages of the common lizard (Zootoca vivipara) are found adjacent to each other. We take advantage of this shared environment to investigate parity-specific dispersal patterns using high-resolution, individual-level spatial-genetic autocorrelation and population genomic approaches (11,726 single nucleotide polymorphisms; 293 oviparous and 310 viviparous individuals). We found isolation-by-distance patterns to be present in both the oviparous and viviparous populations. Density was 2.5 times higher in the oviparous population than the viviparous one, though heterozygosity and genetic diversity measures were similar in the two populations. We found marked differences in the extent of genetic neighbourhoods between the lineages, with the viviparous population showing both dispersal (σ) and spatial-genetic autocorrelation (Moran's I) at 2-fold greater geographic distances than the oviparous population. We found clear evidence of male-biased dispersal from genetic estimates in the viviparous population. In the oviparous population, evidence of male-biased dispersal was weak or absent. These differences are likely to be closely linked to specific requirements of the alternative reproductive strategies and may be the demographic consequences of mother-offspring interactions. Fine-scale geographic and individual-level measures are essential to understanding parity mode differences at microevolutionary scales and to better identifying their ecological and evolutionary impacts.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"70-82"},"PeriodicalIF":2.1,"publicationDate":"2025-01-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142479517","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}
{"title":"Correction to: Tangled banks, braided rivers, and complex hierarchies: beyond microevolution and macroevolution.","authors":"","doi":"10.1093/jeb/voae126","DOIUrl":"10.1093/jeb/voae126","url":null,"abstract":"","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"140"},"PeriodicalIF":2.1,"publicationDate":"2025-01-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142523544","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}
Luis Rodrigo Arce-Valdés, Andrea Viviana Ballén-Guapacha, Anais Rivas-Torres, Jesús Ramsés Chávez-Ríos, Maren Wellenreuther, Bengt Hansson, Rosa Ana Sánchez Guillén
Theoretical work suggests that reinforcement can cause the strengthening of prezygotic isolation in sympatry by mitigating the costs of maladaptive hybridization. However, only a handful of studies have simultaneously tested multiple predictions of this theory in natural populations. We investigated reinforcement in a mottled hybrid zone between the damselflies Ischnura elegans and Ischnura graellsii, which are characterized by incomplete and asymmetric reproductive isolation and exhibit reproductive character displacement in mating-related structures. We tested the conditions for reinforcement by quantifying whether hybridization was costly and prezygotic isolation stronger in sympatry compared with allopatry. Additionally, we investigated two specific predictions of reinforcement: (a) greater premating asymmetries in sympatry; and (b) weaker postzygotic isolation in sympatry than in allopatry. Our findings indicate the presence of maladaptive hybrids, which suggests Bateson-Dobzhansky-Müller incompatibilities in allopatry. We also found that reinforcement has strengthened mechanical isolation, at least in one direction in sympatry. We observed evidence for greater premating asymmetries in sympatry than in allopatry, which is consistent with reinforcement. However, fully testing the prediction of weaker postzygotic isolation in sympatry compared to allopatry was hindered by the highly asymmetrical levels of reproductive isolation between the two reciprocal cross directions. Our study highlights a case where reinforcement and heterospecific gene flow exert opposite effects on reproductive isolation between reciprocal crosses, where reinforcement increases reproductive isolation in one direction while gene flow weakens it in the opposite direction.
{"title":"Testing the predictions of reinforcement: long-term empirical data from a damselfly mottled hybrid zone.","authors":"Luis Rodrigo Arce-Valdés, Andrea Viviana Ballén-Guapacha, Anais Rivas-Torres, Jesús Ramsés Chávez-Ríos, Maren Wellenreuther, Bengt Hansson, Rosa Ana Sánchez Guillén","doi":"10.1093/jeb/voae124","DOIUrl":"10.1093/jeb/voae124","url":null,"abstract":"<p><p>Theoretical work suggests that reinforcement can cause the strengthening of prezygotic isolation in sympatry by mitigating the costs of maladaptive hybridization. However, only a handful of studies have simultaneously tested multiple predictions of this theory in natural populations. We investigated reinforcement in a mottled hybrid zone between the damselflies Ischnura elegans and Ischnura graellsii, which are characterized by incomplete and asymmetric reproductive isolation and exhibit reproductive character displacement in mating-related structures. We tested the conditions for reinforcement by quantifying whether hybridization was costly and prezygotic isolation stronger in sympatry compared with allopatry. Additionally, we investigated two specific predictions of reinforcement: (a) greater premating asymmetries in sympatry; and (b) weaker postzygotic isolation in sympatry than in allopatry. Our findings indicate the presence of maladaptive hybrids, which suggests Bateson-Dobzhansky-Müller incompatibilities in allopatry. We also found that reinforcement has strengthened mechanical isolation, at least in one direction in sympatry. We observed evidence for greater premating asymmetries in sympatry than in allopatry, which is consistent with reinforcement. However, fully testing the prediction of weaker postzygotic isolation in sympatry compared to allopatry was hindered by the highly asymmetrical levels of reproductive isolation between the two reciprocal cross directions. Our study highlights a case where reinforcement and heterospecific gene flow exert opposite effects on reproductive isolation between reciprocal crosses, where reinforcement increases reproductive isolation in one direction while gene flow weakens it in the opposite direction.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"10-27"},"PeriodicalIF":2.1,"publicationDate":"2025-01-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142331497","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}
There is overwhelming evidence that the microbiome can be important to host physiology and fitness. As such, there is interest in and some theoretical work on understanding when hosts and microbiomes (co)evolve so that microbes benefit hosts and hosts favour beneficial microbes. However, the outcome of evolution likely depends on how microbes benefit hosts. Here, we use adaptive dynamics to investigate how host and symbiont evolution depend on whether symbionts increase host lifespan or host reproduction in a simple model of host and symbiont dynamics. In addition, we investigate 2 ways hosts release (and transmit) symbionts: by releasing symbionts steadily during their lifetime or by releasing them at reproduction, potentially increasing symbionts' chances of infecting the host's offspring. The former is strict horizontal transmission, whereas the latter is also a form of indirect or "pseudovertical" transmission. Our first key result is that the evolution of symbionts that benefit host fecundity requires pseudovertical transmission, while the evolution of symbionts that benefit host lifespan does not. Furthermore, our second key result is that when investing in host benefits is costly to the free-living symbiont stage, intermediate levels of pseudovertical transmission are needed for selection to favour beneficial symbionts. This is true regardless of fitness effects because release at reproduction increases the free-living symbiont population, which increases competition for hosts. Consequently, hosts could evolve away from traits that favour beneficial symbionts. Generally, our work emphasizes the importance of different forms of vertical transmission and fitness benefits in host, microbiome, and holobiont evolution as highlighted by our prediction that the evolution of fecundity-increasing symbionts requires parent-to-offspring transmission.
{"title":"How host-microbiome/holobiont evolution depends on whether the microbiome affects host lifespan or fecundity.","authors":"Alexandra L Brown, Britt Koskella, Mike Boots","doi":"10.1093/jeb/voae127","DOIUrl":"10.1093/jeb/voae127","url":null,"abstract":"<p><p>There is overwhelming evidence that the microbiome can be important to host physiology and fitness. As such, there is interest in and some theoretical work on understanding when hosts and microbiomes (co)evolve so that microbes benefit hosts and hosts favour beneficial microbes. However, the outcome of evolution likely depends on how microbes benefit hosts. Here, we use adaptive dynamics to investigate how host and symbiont evolution depend on whether symbionts increase host lifespan or host reproduction in a simple model of host and symbiont dynamics. In addition, we investigate 2 ways hosts release (and transmit) symbionts: by releasing symbionts steadily during their lifetime or by releasing them at reproduction, potentially increasing symbionts' chances of infecting the host's offspring. The former is strict horizontal transmission, whereas the latter is also a form of indirect or \"pseudovertical\" transmission. Our first key result is that the evolution of symbionts that benefit host fecundity requires pseudovertical transmission, while the evolution of symbionts that benefit host lifespan does not. Furthermore, our second key result is that when investing in host benefits is costly to the free-living symbiont stage, intermediate levels of pseudovertical transmission are needed for selection to favour beneficial symbionts. This is true regardless of fitness effects because release at reproduction increases the free-living symbiont population, which increases competition for hosts. Consequently, hosts could evolve away from traits that favour beneficial symbionts. Generally, our work emphasizes the importance of different forms of vertical transmission and fitness benefits in host, microbiome, and holobiont evolution as highlighted by our prediction that the evolution of fecundity-increasing symbionts requires parent-to-offspring transmission.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"41-49"},"PeriodicalIF":2.1,"publicationDate":"2025-01-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142606974","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}
Amino acid substitution models play an important role in studying the evolutionary relationships among species from protein sequences. The amino acid substitution model consists of a large number of parameters; therefore, it is estimated from hundreds or thousands of alignments. Both general models and clade-specific models have been estimated and widely used in phylogenetic analyses. The maximum likelihood method is normally used to select the best-fit model for a specific protein alignment under the study. A number of studies have discussed theoretical concerns as well as the computational burden of the maximum likelihood methods in model selection. Recently, machine learning methods have been proposed for selecting nucleotide models. In this article, we propose a method to measure substitution rates among amino acids (called summary statistics) from protein alignments to efficiently train a deep learning network of so-called ModelDetector for detecting amino acid substitution models. The ModelDetector network was trained from 2,246,400 alignments on a computer with eight cores (without GPU) in about 3.3 hr. Experiments on simulation data showed that the accuracy of the ModelDetector was comparable with that of the maximum likelihood method ModelFinder. It was orders of magnitude faster than the maximum likelihood method in inferring amino acid substitution models and able to analyze genome alignments with millions of sites in minutes. The results indicate that the deep learning network can play as a promising tool for amino acid substitution model selection.
{"title":"An efficient deep learning method for amino acid substitution model selection.","authors":"Nguyen Huy Tinh, Le Sy Vinh","doi":"10.1093/jeb/voae141","DOIUrl":"10.1093/jeb/voae141","url":null,"abstract":"<p><p>Amino acid substitution models play an important role in studying the evolutionary relationships among species from protein sequences. The amino acid substitution model consists of a large number of parameters; therefore, it is estimated from hundreds or thousands of alignments. Both general models and clade-specific models have been estimated and widely used in phylogenetic analyses. The maximum likelihood method is normally used to select the best-fit model for a specific protein alignment under the study. A number of studies have discussed theoretical concerns as well as the computational burden of the maximum likelihood methods in model selection. Recently, machine learning methods have been proposed for selecting nucleotide models. In this article, we propose a method to measure substitution rates among amino acids (called summary statistics) from protein alignments to efficiently train a deep learning network of so-called ModelDetector for detecting amino acid substitution models. The ModelDetector network was trained from 2,246,400 alignments on a computer with eight cores (without GPU) in about 3.3 hr. Experiments on simulation data showed that the accuracy of the ModelDetector was comparable with that of the maximum likelihood method ModelFinder. It was orders of magnitude faster than the maximum likelihood method in inferring amino acid substitution models and able to analyze genome alignments with millions of sites in minutes. The results indicate that the deep learning network can play as a promising tool for amino acid substitution model selection.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"129-139"},"PeriodicalIF":2.1,"publicationDate":"2025-01-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142644072","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 evolutionary game theory, a relative comparison of the cost and benefit associated with obtaining a resource, called payoff, is used as an indicator of fitness of an organism. Payoffs of different strategies, quantitatively represented as payoff matrices, are used to understand complex inter-species and intra-species interactions like cooperation, mutualism, and altruism. Payoff matrices, however, are usually treated as invariant with time-largely due to the absence of any empirical data quantifying their evolution. In this paper, we present empirical evidence of three types of resource-dependent changes in the payoff matrices of evolving Saccharomyces cerevisiae populations. We show that depending on the carbon source and participating genotypes, N-player games could collapse, be born, or be maintained. Our results highlight the need to consider the dynamic nature of payoff matrices while making even short-term predictions about population interactions and dynamics.
{"title":"Empirical evidence of resource dependent evolution of payoff matrices in Saccharomyces cerevisiae populations.","authors":"Pavithra Venkataraman, Anjali Mahilkar, Namratha Raj, Supreet Saini","doi":"10.1093/jeb/voae128","DOIUrl":"10.1093/jeb/voae128","url":null,"abstract":"<p><p>In evolutionary game theory, a relative comparison of the cost and benefit associated with obtaining a resource, called payoff, is used as an indicator of fitness of an organism. Payoffs of different strategies, quantitatively represented as payoff matrices, are used to understand complex inter-species and intra-species interactions like cooperation, mutualism, and altruism. Payoff matrices, however, are usually treated as invariant with time-largely due to the absence of any empirical data quantifying their evolution. In this paper, we present empirical evidence of three types of resource-dependent changes in the payoff matrices of evolving Saccharomyces cerevisiae populations. We show that depending on the carbon source and participating genotypes, N-player games could collapse, be born, or be maintained. Our results highlight the need to consider the dynamic nature of payoff matrices while making even short-term predictions about population interactions and dynamics.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":"122-128"},"PeriodicalIF":2.1,"publicationDate":"2025-01-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11696675/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142394849","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}