Pub Date : 2024-10-10eCollection Date: 2025-02-01DOI: 10.1093/evlett/qrae051
Francesca Santostefano, Maria Moiron, Alfredo Sánchez-Tójar, David N Fisher
The evolutionary potential of traits is governed by the amount of heritable variation available to selection. While this is typically quantified based on genetic variation in a focal individual for its own traits (direct genetic effects, DGEs), when social interactions occur, genetic variation in interacting partners can influence a focal individual's traits (indirect genetic effects, IGEs). Theory and studies on domesticated species have suggested IGEs can greatly impact evolutionary trajectories, but whether this is true more broadly remains unclear. Here, we perform a systematic review and meta-analysis to quantify the amount of trait variance explained by IGEs and the contribution of IGEs to predictions of adaptive potential. We identified 180 effect sizes from 47 studies across 21 species and found that, on average, IGEs of a single social partner account for a small but statistically significant amount of phenotypic variation (0.03). As IGEs affect the trait values of each interacting group member and due to a typically positive-although statistically nonsignificant-correlation with DGEs (rDGE-IGE = 0.26), IGEs ultimately increase trait heritability substantially from 0.27 (narrow-sense heritability) to 0.45 (total heritable variance). This 66% average increase in heritability suggests IGEs can increase the amount of genetic variation available to selection. Furthermore, whilst showing considerable variation across studies, IGEs were most prominent for behaviors and, to a lesser extent, for reproduction and survival, in contrast to morphological, metabolic, physiological, and development traits. Our meta-analysis, therefore, shows that IGEs tend to enhance the evolutionary potential of traits, especially for those tightly related to interactions with other individuals, such as behavior and reproduction.
{"title":"Indirect genetic effects increase the heritable variation available to selection and are largest for behaviors: a meta-analysis.","authors":"Francesca Santostefano, Maria Moiron, Alfredo Sánchez-Tójar, David N Fisher","doi":"10.1093/evlett/qrae051","DOIUrl":"10.1093/evlett/qrae051","url":null,"abstract":"<p><p>The evolutionary potential of traits is governed by the amount of heritable variation available to selection. While this is typically quantified based on genetic variation in a focal individual for its own traits (direct genetic effects, DGEs), when social interactions occur, genetic variation in interacting partners can influence a focal individual's traits (indirect genetic effects, IGEs). Theory and studies on domesticated species have suggested IGEs can greatly impact evolutionary trajectories, but whether this is true more broadly remains unclear. Here, we perform a systematic review and meta-analysis to quantify the amount of trait variance explained by IGEs and the contribution of IGEs to predictions of adaptive potential. We identified 180 effect sizes from 47 studies across 21 species and found that, on average, IGEs of a single social partner account for a small but statistically significant amount of phenotypic variation (0.03). As IGEs affect the trait values of each interacting group member and due to a typically positive-although statistically nonsignificant-correlation with DGEs (<i>r</i> <sub>DGE-IGE</sub> = 0.26), IGEs ultimately increase trait heritability substantially from 0.27 (narrow-sense heritability) to 0.45 (total heritable variance). This 66% average increase in heritability suggests IGEs can increase the amount of genetic variation available to selection. Furthermore, whilst showing considerable variation across studies, IGEs were most prominent for behaviors and, to a lesser extent, for reproduction and survival, in contrast to morphological, metabolic, physiological, and development traits. Our meta-analysis, therefore, shows that IGEs tend to enhance the evolutionary potential of traits, especially for those tightly related to interactions with other individuals, such as behavior and reproduction.</p>","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"9 1","pages":"89-104"},"PeriodicalIF":3.4,"publicationDate":"2024-10-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11790215/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143190851","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-08eCollection Date: 2025-02-01DOI: 10.1093/evlett/qrae046
Alexus S Roberts-Hugghis, Christopher M Martinez, Katherine A Corn, Peter C Wainwright
Modifications to the pharyngeal jaws-a prey processing system located posterior to the mouth cavity-are widely considered a key innovation that enhanced diversification within several prominent fish clades. Seen in cichlids, damselfishes, wrasses, and a few other lineages, these musculoskeletal alterations are believed to increase the evolutionary independence and, thus, the diversification of the oral and pharyngeal jaw systems. To test this classic hypothesis, we conducted comparative phylogenetic analyses to assess the effect of the pharyngeal novelty on the diversification of feeding morphology and kinematics across a taxonomically diverse sample of spiny-rayed fishes. We quantified movements of the oral jaws and other craniofacial structures from 689 suction-feeding strikes using high-speed videos collected from 228 species with and without the pharyngeal jaw novelty. Contradicting long-held predictions, we find significantly greater disparity across all traits and faster rates of oral jaw functional evolution in fishes without the specialized prey processing system. The modified pharyngeal jaw is undoubtedly a functional innovation as it enhances the strength of the prey processing system, facilitating exceptional transition rates to feeding on hard and tough prey. However, it also restricts the diversification of the feeding system, revealing that the impact of pharyngognathy is more nuanced than previously thought. In light of these and other recent findings, a reinterpretation of the macroevolutionary consequences of the pharyngeal jaw novelty is needed.
{"title":"A classic key innovation constrains oral jaw functional diversification in fishes.","authors":"Alexus S Roberts-Hugghis, Christopher M Martinez, Katherine A Corn, Peter C Wainwright","doi":"10.1093/evlett/qrae046","DOIUrl":"10.1093/evlett/qrae046","url":null,"abstract":"<p><p>Modifications to the pharyngeal jaws-a prey processing system located posterior to the mouth cavity-are widely considered a key innovation that enhanced diversification within several prominent fish clades. Seen in cichlids, damselfishes, wrasses, and a few other lineages, these musculoskeletal alterations are believed to increase the evolutionary independence and, thus, the diversification of the oral and pharyngeal jaw systems. To test this classic hypothesis, we conducted comparative phylogenetic analyses to assess the effect of the pharyngeal novelty on the diversification of feeding morphology and kinematics across a taxonomically diverse sample of spiny-rayed fishes. We quantified movements of the oral jaws and other craniofacial structures from 689 suction-feeding strikes using high-speed videos collected from 228 species with and without the pharyngeal jaw novelty. Contradicting long-held predictions, we find significantly greater disparity across all traits and faster rates of oral jaw functional evolution in fishes without the specialized prey processing system. The modified pharyngeal jaw is undoubtedly a functional innovation as it enhances the strength of the prey processing system, facilitating exceptional transition rates to feeding on hard and tough prey. However, it also restricts the diversification of the feeding system, revealing that the impact of pharyngognathy is more nuanced than previously thought. In light of these and other recent findings, a reinterpretation of the macroevolutionary consequences of the pharyngeal jaw novelty is needed.</p>","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"9 1","pages":"24-40"},"PeriodicalIF":3.4,"publicationDate":"2024-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11790220/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143190375","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-08eCollection Date: 2025-02-01DOI: 10.1093/evlett/qrae049
G Sander van Doorn, Jens Schepers, Roelof A Hut, Astrid T Groot
Noctuid moths provide prime examples of species in various stages of allochronic speciation, where reproductive barriers are mediated by genetic divergence in daily or seasonal timing. Theory indicates that allochronic divergence might be one of the most plausible mechanisms of adaptive speciation, especially when timing is subject to divergent ecological selection. Here, we show that the validity of this theoretical expectation is entirely contingent on species characteristics of the mating system. Our analysis focuses on the moth Spodoptera frugiperda (Lepidoptera, Noctuidae), which occurs as two strains that differ in circadian reproductive activity. Unlike in generic models of assortative mating, where chronotypes diverge under mild assumptions, individual-based evolutionary simulations of the mating system and life cycle of S. frugiperda fail to recover allochronic diversification, even under conditions highly conducive to speciation. Instead, we observe that both chronotypes advance their activity schedule toward the early night, resulting in a rapid loss of allochronic variation. This outcome is caused by the fact that mating in S. frugiperda takes considerable time and potential mates are encountered sequentially, so that early males enjoy a systematic advantage. The undermining effect of male mate competition can be overcome when circadian genes evolve sex-specific expression, enabling early and late chronotypes to be maintained or even to diversify in sympatry. These results give new significance to sex differences in biological rhythms and suggest that species characteristics of the mating system and genetic architecture are key to understanding the scope for allochronic speciation across diverse species exhibiting variation in timing.
{"title":"Sex-specific expression of circadian rhythms enables allochronic speciation.","authors":"G Sander van Doorn, Jens Schepers, Roelof A Hut, Astrid T Groot","doi":"10.1093/evlett/qrae049","DOIUrl":"10.1093/evlett/qrae049","url":null,"abstract":"<p><p>Noctuid moths provide prime examples of species in various stages of allochronic speciation, where reproductive barriers are mediated by genetic divergence in daily or seasonal timing. Theory indicates that allochronic divergence might be one of the most plausible mechanisms of adaptive speciation, especially when timing is subject to divergent ecological selection. Here, we show that the validity of this theoretical expectation is entirely contingent on species characteristics of the mating system. Our analysis focuses on the moth <i>Spodoptera frugiperda</i> (Lepidoptera, Noctuidae), which occurs as two strains that differ in circadian reproductive activity. Unlike in generic models of assortative mating, where chronotypes diverge under mild assumptions, individual-based evolutionary simulations of the mating system and life cycle of <i>S. frugiperda</i> fail to recover allochronic diversification, even under conditions highly conducive to speciation. Instead, we observe that both chronotypes advance their activity schedule toward the early night, resulting in a rapid loss of allochronic variation. This outcome is caused by the fact that mating in <i>S. frugiperda</i> takes considerable time and potential mates are encountered sequentially, so that early males enjoy a systematic advantage. The undermining effect of male mate competition can be overcome when circadian genes evolve sex-specific expression, enabling early and late chronotypes to be maintained or even to diversify in sympatry. These results give new significance to sex differences in biological rhythms and suggest that species characteristics of the mating system and genetic architecture are key to understanding the scope for allochronic speciation across diverse species exhibiting variation in timing.</p>","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"9 1","pages":"65-76"},"PeriodicalIF":3.4,"publicationDate":"2024-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11790224/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143190872","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-26eCollection Date: 2025-02-01DOI: 10.1093/evlett/qrae050
Diana Tataru, Max De Leon, Spencer Dutton, Fidel Machado Perez, Alexander Rendahl, Kathleen G Ferris
While hybridization was viewed as a hindrance to adaptation and speciation by early evolutionary biologists, recent studies have demonstrated the importance of hybridization in facilitating evolutionary processes. However, it is still not well-known what role spatial and temporal variation in natural selection play in the maintenance of naturally occurring hybrid zones. To identify whether hybridization is adaptive between two closely related monkeyflower species, Mimulus guttatus and Mimulus laciniatus, we performed repeated reciprocal transplants between natural hybrid and pure species' populations. We planted parental genotypes along with multiple experimental hybrid generations in a dry (2021) and extremely wet (2023) year in the Sierra Nevada, CA. By taking fine-scale environmental measurements, we found that the environment of the hybrid zone is more similar to M. laciniatus's seasonally dry rocky outcrop habitat than M. guttatus's moist meadows. In our transplants hybridization does not appear to be maintained by a consistent fitness advantage of hybrids over parental species in hybrid zones, but rather a lack of strong selection against hybrids. We also found higher fitness of the drought-adapted species, M. laciniatus, than M. guttatus in both species' habitats, as well as phenotypic selection for M. laciniatus-like traits in the hybrid habitat in the dry year of our experiment. These findings suggest that in this system, hybridization might function to introduce drought-adapted traits and genes from M. laciniatus into M. guttatus, specifically in years with limited soil moisture. However, we also find evidence of genetic incompatibilities in second generation hybrids in the wetter year, which may balance a selective advantage of M. laciniatus introgression. Therefore, we find that hybridization in this system is both potentially adaptive and costly, and that the interaction of positive and negative selection likely determines patterns of gene flow between these Mimulus species.
{"title":"Fluctuating selection in a monkeyflower hybrid zone.","authors":"Diana Tataru, Max De Leon, Spencer Dutton, Fidel Machado Perez, Alexander Rendahl, Kathleen G Ferris","doi":"10.1093/evlett/qrae050","DOIUrl":"10.1093/evlett/qrae050","url":null,"abstract":"<p><p>While hybridization was viewed as a hindrance to adaptation and speciation by early evolutionary biologists, recent studies have demonstrated the importance of hybridization in facilitating evolutionary processes. However, it is still not well-known what role spatial and temporal variation in natural selection play in the maintenance of naturally occurring hybrid zones. To identify whether hybridization is adaptive between two closely related monkeyflower species, <i>Mimulus guttatus</i> and <i>Mimulus laciniatus</i>, we performed repeated reciprocal transplants between natural hybrid and pure species' populations. We planted parental genotypes along with multiple experimental hybrid generations in a dry (2021) and extremely wet (2023) year in the Sierra Nevada, CA. By taking fine-scale environmental measurements, we found that the environment of the hybrid zone is more similar to <i>M. laciniatus's</i> seasonally dry rocky outcrop habitat than <i>M. guttatus's</i> moist meadows. In our transplants hybridization does not appear to be maintained by a consistent fitness advantage of hybrids over parental species in hybrid zones, but rather a lack of strong selection against hybrids. We also found higher fitness of the drought-adapted species, <i>M. laciniatus,</i> than <i>M. guttatus</i> in both species' habitats, as well as phenotypic selection for <i>M. laciniatus-</i>like traits in the hybrid habitat in the dry year of our experiment. These findings suggest that in this system, hybridization might function to introduce drought-adapted traits and genes from <i>M. laciniatus</i> into <i>M. guttatus</i>, specifically in years with limited soil moisture. However, we also find evidence of genetic incompatibilities in second generation hybrids in the wetter year, which may balance a selective advantage of <i>M. laciniatus</i> introgression. Therefore, we find that hybridization in this system is both potentially adaptive and costly, and that the interaction of positive and negative selection likely determines patterns of gene flow between these <i>Mimulus</i> species.</p>","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"9 1","pages":"77-88"},"PeriodicalIF":3.4,"publicationDate":"2024-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11790225/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143190827","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-22eCollection Date: 2025-02-01DOI: 10.1093/evlett/qrae047
Nina Serén, Catarina Pinho, Rodrigo Megía-Palma, Prem Aguilar, Anamarija Žagar, Pedro Andrade, Miguel A Carretero
High altitude imposes several extreme constraints on life, such as low oxygen pressure and high levels of ultraviolet radiation, which require specialized adaptations. Many studies have focused on how endothermic vertebrates respond to these challenging environments, but there is still uncertainty on how ectotherms adapt to these conditions. Here, we used whole-genome sequencing of low-altitude (100-600 m) and high-altitude (3,550 m) populations of the wide-ranging Tenerife lizard Gallotia galloti to uncover signatures of selection for altitudinal adaptation. The studied populations show reduced differentiation, sharing similar patterns of genetic variation. Selective sweep mapping suggests that signatures of adaptation to high altitude are not widespread across the genome, clustering in a relatively small number of genomic regions. One of these regions contains BMPER, a gene involved with vascular remodeling, and that has been associated with hypoxia-induced angiogenic response. By genotyping samples across 2 altitudinal transects, we show that allele frequency changes at this locus are not gradual, but rather show a well-defined shift above ca. 1,900 m. Transcript and protein structure analyses on this gene suggest that putative selection likely acts on noncoding variation. These results underline how low oxygen pressure generates the most consistent selective constraint in high-altitude environments, to which vertebrates with vastly contrasting physiological profiles need to adapt in the context of ongoing climate change.
{"title":"Selection on the vascular-remodeling <i>BMPER</i> gene is associated with altitudinal adaptation in an insular lizard.","authors":"Nina Serén, Catarina Pinho, Rodrigo Megía-Palma, Prem Aguilar, Anamarija Žagar, Pedro Andrade, Miguel A Carretero","doi":"10.1093/evlett/qrae047","DOIUrl":"10.1093/evlett/qrae047","url":null,"abstract":"<p><p>High altitude imposes several extreme constraints on life, such as low oxygen pressure and high levels of ultraviolet radiation, which require specialized adaptations. Many studies have focused on how endothermic vertebrates respond to these challenging environments, but there is still uncertainty on how ectotherms adapt to these conditions. Here, we used whole-genome sequencing of low-altitude (100-600 m) and high-altitude (3,550 m) populations of the wide-ranging Tenerife lizard <i>Gallotia galloti</i> to uncover signatures of selection for altitudinal adaptation. The studied populations show reduced differentiation, sharing similar patterns of genetic variation. Selective sweep mapping suggests that signatures of adaptation to high altitude are not widespread across the genome, clustering in a relatively small number of genomic regions. One of these regions contains <i>BMPER</i>, a gene involved with vascular remodeling, and that has been associated with hypoxia-induced angiogenic response. By genotyping samples across 2 altitudinal transects, we show that allele frequency changes at this locus are not gradual, but rather show a well-defined shift above ca. 1,900 m. Transcript and protein structure analyses on this gene suggest that putative selection likely acts on noncoding variation. These results underline how low oxygen pressure generates the most consistent selective constraint in high-altitude environments, to which vertebrates with vastly contrasting physiological profiles need to adapt in the context of ongoing climate change.</p>","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"9 1","pages":"41-50"},"PeriodicalIF":3.4,"publicationDate":"2024-09-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11790214/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143190871","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-22eCollection Date: 2025-02-01DOI: 10.1093/evlett/qrae048
Leonel Herrera-Alsina, Rossina Parvanova, Jacinta Guirguis, Greta Bocedi, Liam Trethowan, Lesley T Lancaster, Justin M J Travis
Despite the high importance and risk of mountain ecosystems in global biodiversity conservation, the mechanisms giving rise to and maintaining elevational biodiversity gradients are poorly understood, limiting predictions of future responses. Species richness peaks at lowlands for many taxa, which might be a consequence of mountain shape, reducing available area in highlands. For other taxa, diversity can be highest at mid elevations, suggesting the presence of mechanisms that counteract the influence of geometry. Here, we mechanistically investigate the role of mountain geometry (smaller at the peak) interaction with ecological niche width, diversification, and altitudinal dispersal to investigate the relative roles of these processes in shaping elevational biodiversity gradients. We simulated landscapes and lineages until species richness stop increasing and showed that the disproportionately large area of lowlands provides opportunity for higher species accumulation than any other elevation, even when available niche width and per-capita diversification rate are uniform across altitudes. Regardless of the underlying Elevational Diversity Gradient, altitudinal dispersal always plays a stronger role in maintaining highland than lowland diversity, due to unequal areas involved. To empirically test these predictions resulting from our model, we fit dynamic models of diversification and altitudinal dispersal to three mountainous endemic radiations whose species richness peaks in mid and high-elevation. We find that highland diversity is explained by increased diversification rates with elevation in Fijian bees, whereas niche availability is more likely to explain high altitude diversity in frailejon bushes and earless frogs, suggesting these clades are still growing. Our model and findings provide a new framework for distinguishing drivers of diversity dynamics on mountainsides and allow to detect the presence of clade-specific mechanisms underlying the geometry-diversity relationship. Understanding of these ecological and evolutionary forces can allow increased predictability of how ongoing land use and climate changes will impact future highland biodiversity.
{"title":"Disentangling evolutionary, geometric and ecological components of the elevational gradient of diversity.","authors":"Leonel Herrera-Alsina, Rossina Parvanova, Jacinta Guirguis, Greta Bocedi, Liam Trethowan, Lesley T Lancaster, Justin M J Travis","doi":"10.1093/evlett/qrae048","DOIUrl":"10.1093/evlett/qrae048","url":null,"abstract":"<p><p>Despite the high importance and risk of mountain ecosystems in global biodiversity conservation, the mechanisms giving rise to and maintaining elevational biodiversity gradients are poorly understood, limiting predictions of future responses. Species richness peaks at lowlands for many taxa, which might be a consequence of mountain shape, reducing available area in highlands. For other taxa, diversity can be highest at mid elevations, suggesting the presence of mechanisms that counteract the influence of geometry. Here, we mechanistically investigate the role of mountain geometry (smaller at the peak) interaction with ecological niche width, diversification, and altitudinal dispersal to investigate the relative roles of these processes in shaping elevational biodiversity gradients. We simulated landscapes and lineages until species richness stop increasing and showed that the disproportionately large area of lowlands provides opportunity for higher species accumulation than any other elevation, even when available niche width and per-capita diversification rate are uniform across altitudes. Regardless of the underlying Elevational Diversity Gradient, altitudinal dispersal always plays a stronger role in maintaining highland than lowland diversity, due to unequal areas involved. To empirically test these predictions resulting from our model, we fit dynamic models of diversification and altitudinal dispersal to three mountainous endemic radiations whose species richness peaks in mid and high-elevation. We find that highland diversity is explained by increased diversification rates with elevation in Fijian bees, whereas niche availability is more likely to explain high altitude diversity in frailejon bushes and earless frogs, suggesting these clades are still growing. Our model and findings provide a new framework for distinguishing drivers of diversity dynamics on mountainsides and allow to detect the presence of clade-specific mechanisms underlying the geometry-diversity relationship. Understanding of these ecological and evolutionary forces can allow increased predictability of how ongoing land use and climate changes will impact future highland biodiversity.</p>","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"9 1","pages":"51-64"},"PeriodicalIF":3.4,"publicationDate":"2024-09-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11790213/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143190681","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-17eCollection Date: 2024-12-01DOI: 10.1093/evlett/qrae033
Tom R Booker
Environmental heterogeneity can lead to spatially varying selection, which can, in turn, lead to local adaptation. Population genetic models have shown that the pattern of environmental variation in space can strongly influence the evolution of local adaptation. In particular, when environmental variation is highly autocorrelated in space local adaptation will more readily evolve. However, there have been few attempts to test this prediction empirically or characterize the consequences it would have for the genetic architecture underlying local adaptation. In this study, I analyze a large-scale provenance trial conducted on lodgepole pine and find suggestive evidence that spatial autocorrelation in environmental variation is related to the strength of local adaptation that has evolved in that species. Motivated by those results, I use simulations to model local adaptation to different spatial patterns of environmental variation. The simulations confirm that local adaptation is expected to increase with the degree of spatial autocorrelation in the selective environment, but also show that highly heterogeneous environments are more likely to exhibit high variation in local adaptation, a result not previously described. I find that the spatial pattern of environmental variation influences the genetic architectures underlying local adaptation. In highly autocorrelated environments, the genetic architecture of local adaptation tends to be composed of high-frequency alleles with small phenotypic effects. In weakly autocorrelated environments, locally adaptive alleles may have larger phenotypic effects but are present at lower frequencies across species' ranges and experience more evolutionary turnover. Overall, this work emphasizes the profound importance that the spatial pattern of selection can have on the evolution of local adaptation and how spatial autocorrelation should be considered when formulating hypotheses in ecological and genetic studies.
{"title":"The structure of the environment influences the patterns and genetics of local adaptation.","authors":"Tom R Booker","doi":"10.1093/evlett/qrae033","DOIUrl":"10.1093/evlett/qrae033","url":null,"abstract":"<p><p>Environmental heterogeneity can lead to spatially varying selection, which can, in turn, lead to local adaptation. Population genetic models have shown that the pattern of environmental variation in space can strongly influence the evolution of local adaptation. In particular, when environmental variation is highly autocorrelated in space local adaptation will more readily evolve. However, there have been few attempts to test this prediction empirically or characterize the consequences it would have for the genetic architecture underlying local adaptation. In this study, I analyze a large-scale provenance trial conducted on lodgepole pine and find suggestive evidence that spatial autocorrelation in environmental variation is related to the strength of local adaptation that has evolved in that species. Motivated by those results, I use simulations to model local adaptation to different spatial patterns of environmental variation. The simulations confirm that local adaptation is expected to increase with the degree of spatial autocorrelation in the selective environment, but also show that highly heterogeneous environments are more likely to exhibit high variation in local adaptation, a result not previously described. I find that the spatial pattern of environmental variation influences the genetic architectures underlying local adaptation. In highly autocorrelated environments, the genetic architecture of local adaptation tends to be composed of high-frequency alleles with small phenotypic effects. In weakly autocorrelated environments, locally adaptive alleles may have larger phenotypic effects but are present at lower frequencies across species' ranges and experience more evolutionary turnover. Overall, this work emphasizes the profound importance that the spatial pattern of selection can have on the evolution of local adaptation and how spatial autocorrelation should be considered when formulating hypotheses in ecological and genetic studies.</p>","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"8 6","pages":"787-798"},"PeriodicalIF":3.4,"publicationDate":"2024-08-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11637683/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142830570","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-17eCollection Date: 2024-12-01DOI: 10.1093/evlett/qrae045
Cyril C Grueter, Stefan Lüpold
Gregarious mammals interact to varying degrees and in a variety of ways with neighboring groups. Since navigating this wider social environment via conventional means (social knowledge) may be challenging, we hypothesize that between-group socio-spatial dynamics have exerted strong selection on phenotypic markers of individual identity, quality, and competitive ability. Ornaments are sexually selected decorative traits with far-reaching signaling potential. Here, we examined the links between sexual dimorphism in ornamentation, home range use and encounter rates across 144 primate species in a Bayesian framework. We show that home range overlap (shared space among neighbors), an indicator of the complexity of between-group interactions (but not necessarily male-male competition), is positively associated with dimorphism in ornamentation. We find no clear effect for between-group encounter rates. We also find that inter-group interactions were less agonistic when there was greater home range overlap. Taken together, these findings indicate that ornaments play a hitherto underappreciated role in signaling to conspecifics outside the realms of their home groups.
{"title":"The role of between-group signaling in the evolution of primate ornamentation.","authors":"Cyril C Grueter, Stefan Lüpold","doi":"10.1093/evlett/qrae045","DOIUrl":"10.1093/evlett/qrae045","url":null,"abstract":"<p><p>Gregarious mammals interact to varying degrees and in a variety of ways with neighboring groups. Since navigating this wider social environment via conventional means (social knowledge) may be challenging, we hypothesize that between-group socio-spatial dynamics have exerted strong selection on phenotypic markers of individual identity, quality, and competitive ability. Ornaments are sexually selected decorative traits with far-reaching signaling potential. Here, we examined the links between sexual dimorphism in ornamentation, home range use and encounter rates across 144 primate species in a Bayesian framework. We show that home range overlap (shared space among neighbors), an indicator of the complexity of between-group interactions (but not necessarily male-male competition), is positively associated with dimorphism in ornamentation. We find no clear effect for between-group encounter rates. We also find that inter-group interactions were less agonistic when there was greater home range overlap. Taken together, these findings indicate that ornaments play a hitherto underappreciated role in signaling to conspecifics outside the realms of their home groups.</p>","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"8 6","pages":"927-935"},"PeriodicalIF":3.4,"publicationDate":"2024-08-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11637682/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142830567","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-17eCollection Date: 2024-12-01DOI: 10.1093/evlett/qrae044
Tim Janicke
The Darwin-Bateman paradigm advanced as the central concept to explain the evolutionary origin of sex differences. However, debates regarding its theoretical underpinnings persist, particularly with respect to the role of anisogamy in sexual selection. The theoretical work presented by Lehtonen and Parker suggests that the initial split in gamete production rate drives sex differences in sexual selection but that any further variation in the degree of anisogamy is not expected to alter the strength of sexual selection in males and females. Here, I discuss the historical background of a recently emerged controversy and present empirical data that corroborate the theoretical predictions. Lehtonen and Parker's contribution refines our understanding of the Darwin-Bateman paradigm by providing a broad theory for large-scale patterns of sex differences that can be observed in nature. Further understanding of how demographic and environmental factors influence sexual selection is essential to predict the vast diversity of sex differences across the tree of life, beyond the primordial impact of anisogamy.
{"title":"Anisogamy and the Darwin-Bateman paradigm.","authors":"Tim Janicke","doi":"10.1093/evlett/qrae044","DOIUrl":"10.1093/evlett/qrae044","url":null,"abstract":"<p><p>The Darwin-Bateman paradigm advanced as the central concept to explain the evolutionary origin of sex differences. However, debates regarding its theoretical underpinnings persist, particularly with respect to the role of anisogamy in sexual selection. The theoretical work presented by Lehtonen and Parker suggests that the initial split in gamete production rate drives sex differences in sexual selection but that any further variation in the degree of anisogamy is not expected to alter the strength of sexual selection in males and females. Here, I discuss the historical background of a recently emerged controversy and present empirical data that corroborate the theoretical predictions. Lehtonen and Parker's contribution refines our understanding of the Darwin-Bateman paradigm by providing a broad theory for large-scale patterns of sex differences that can be observed in nature. Further understanding of how demographic and environmental factors influence sexual selection is essential to predict the vast diversity of sex differences across the tree of life, beyond the primordial impact of anisogamy.</p>","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"8 6","pages":"756-760"},"PeriodicalIF":3.4,"publicationDate":"2024-08-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11637679/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142830436","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-14eCollection Date: 2024-12-01DOI: 10.1093/evlett/qrae042
Leeban H Yusuf, Sonia Pascoal, Peter A Moran, Nathan W Bailey
Differences in interspecific mating traits, such as male sexual signals and female preferences, often evolve quickly as initial barriers to gene flow between nascent lineages, and they may also strengthen such barriers during secondary contact via reinforcement. However, it is an open question whether loci contributing to intraspecific variation in sexual traits are co-opted during the formation and strengthening of mating barriers between species. To test this, we used a population genomics approach in natural populations of Australian cricket sister species that overlap in a contact zone: Teleogryllus oceanicus and Teleogryllus commodus. First, we identified loci associated with intraspecific variation in T. oceanicus mating signals: advertisement song and cuticular hydrocarbon (CHC) pheromones. We then separately identified candidate interspecific barrier loci between the species. Genes showing elevated allelic divergence between species were enriched for neurological functions, indicating potential behavioral rewiring. Only two CHC-associated genes overlapped with these interspecific candidate barrier loci, and intraspecific CHC loci showed signatures of being under strong selective constraints between species. In contrast, 10 intraspecific song-associated genes showed high genetic differentiation between T. commodus and T. oceanicus, and 2 had signals of high genomic divergence. The overall lack of shared loci in intra vs. interspecific comparisons of mating trait and candidate barrier loci is consistent with limited co-option of the genetic architecture of interspecific mating signals during the establishment and maintenance of reproductive isolation.
{"title":"Testing the genomic overlap between intraspecific mating traits and interspecific mating barriers.","authors":"Leeban H Yusuf, Sonia Pascoal, Peter A Moran, Nathan W Bailey","doi":"10.1093/evlett/qrae042","DOIUrl":"10.1093/evlett/qrae042","url":null,"abstract":"<p><p>Differences in interspecific mating traits, such as male sexual signals and female preferences, often evolve quickly as initial barriers to gene flow between nascent lineages, and they may also strengthen such barriers during secondary contact via reinforcement. However, it is an open question whether loci contributing to intraspecific variation in sexual traits are co-opted during the formation and strengthening of mating barriers between species. To test this, we used a population genomics approach in natural populations of Australian cricket sister species that overlap in a contact zone: <i>Teleogryllus oceanicus</i> and <i>Teleogryllus commodus.</i> First, we identified loci associated with intraspecific variation in <i>T. oceanicus</i> mating signals: advertisement song and cuticular hydrocarbon (CHC) pheromones. We then separately identified candidate interspecific barrier loci between the species. Genes showing elevated allelic divergence between species were enriched for neurological functions, indicating potential behavioral rewiring. Only two CHC-associated genes overlapped with these interspecific candidate barrier loci, and intraspecific CHC loci showed signatures of being under strong selective constraints between species. In contrast, 10 intraspecific song-associated genes showed high genetic differentiation between <i>T. commodus</i> and <i>T. oceanicus</i>, and 2 had signals of high genomic divergence. The overall lack of shared loci in intra vs. interspecific comparisons of mating trait and candidate barrier loci is consistent with limited co-option of the genetic architecture of interspecific mating signals during the establishment and maintenance of reproductive isolation.</p>","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"8 6","pages":"902-915"},"PeriodicalIF":3.4,"publicationDate":"2024-08-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11637687/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142830476","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}