Pub Date : 2025-10-08DOI: 10.1038/s41437-025-00804-7
Vivak Soni, Cyril J. Versoza, Susanne P. Pfeifer, Jeffrey D. Jensen
The common marmoset (Callithrix jacchus) is of considerable biomedical importance, yet there remains a need to characterize the evolutionary forces shaping empirically observed patterns of genomic variation in the species. However, two uncommon biological traits potentially prevent the use of standard population genetic approaches in this primate: a high frequency of twin births and the prevalence of hematopoietic chimerism. Here we characterize the impact of these biological features on the inference of natural selection, and directly model twinning and chimerism when performing inference of the distribution of fitness effects to characterize general selective dynamics as well as when scanning the genome for loci shaped by the action of episodic positive and balancing selection. Results suggest a generally increased degree of purifying selection relative to human populations, consistent with the larger estimated effective population size of common marmosets. Furthermore, genomic scans based on an appropriate evolutionary baseline model reveal a small number of genes related to immunity, sensory perception, and reproduction to be strong sweep candidates. Notably, two genes in the major histocompatibility complex were found to have strong evidence of being maintained by balancing selection, in agreement with observations in other primate species. Taken together, this work, presenting the first whole-genome characterization of selective dynamics in the common marmoset, thus provides important insights into the landscape of both persistent and episodic selective forces in this species.
{"title":"Investigating the effects of chimerism on the inference of selection: quantifying genomic targets of purifying, positive, and balancing selection in common marmosets (Callithrix jacchus)","authors":"Vivak Soni, Cyril J. Versoza, Susanne P. Pfeifer, Jeffrey D. Jensen","doi":"10.1038/s41437-025-00804-7","DOIUrl":"10.1038/s41437-025-00804-7","url":null,"abstract":"The common marmoset (Callithrix jacchus) is of considerable biomedical importance, yet there remains a need to characterize the evolutionary forces shaping empirically observed patterns of genomic variation in the species. However, two uncommon biological traits potentially prevent the use of standard population genetic approaches in this primate: a high frequency of twin births and the prevalence of hematopoietic chimerism. Here we characterize the impact of these biological features on the inference of natural selection, and directly model twinning and chimerism when performing inference of the distribution of fitness effects to characterize general selective dynamics as well as when scanning the genome for loci shaped by the action of episodic positive and balancing selection. Results suggest a generally increased degree of purifying selection relative to human populations, consistent with the larger estimated effective population size of common marmosets. Furthermore, genomic scans based on an appropriate evolutionary baseline model reveal a small number of genes related to immunity, sensory perception, and reproduction to be strong sweep candidates. Notably, two genes in the major histocompatibility complex were found to have strong evidence of being maintained by balancing selection, in agreement with observations in other primate species. Taken together, this work, presenting the first whole-genome characterization of selective dynamics in the common marmoset, thus provides important insights into the landscape of both persistent and episodic selective forces in this species.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"134 10-11","pages":"645-657"},"PeriodicalIF":3.9,"publicationDate":"2025-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12577292/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145250856","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"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 : 2025-10-01DOI: 10.1038/s41437-025-00801-w
Adam Z. Hasik, Anna M. Hewett, Katie Maris, Sean J. Morris, Ali Morris, Gregory F. Albery, Josephine M. Pemberton
Inbreeding depression is the reduction in fitness of inbred individuals relative to their more outbred counterparts. Parasitism also reduces fitness and is a route by which inbreeding depression may operate, yet the complete pathway from inbreeding to parasitism to fitness has almost never been documented in the wild. We investigated parasite-mediated inbreeding depression in a wild population of a large mammal (red deer, Cervus elaphus), using high-quality individual-level data on fitness in juveniles and adult females, longitudinal infection data for three gastrointestinal helminth parasites, and genomic inbreeding coefficients. We found evidence for parasite-mediated inbreeding depression via strongyle nematodes in juvenile survival, independent of direct adverse effects of inbreeding on survival and indirect effects of inbreeding on survival via birth weight. Inbreeding also reduced fitness in reproductive adults by reducing overwinter survival. Our study reveals three independent pathways by which inbreeding depresses fitness and highlights the rarely-studied route of parasitism.
{"title":"Parasite-mediated inbreeding depression in wild red deer","authors":"Adam Z. Hasik, Anna M. Hewett, Katie Maris, Sean J. Morris, Ali Morris, Gregory F. Albery, Josephine M. Pemberton","doi":"10.1038/s41437-025-00801-w","DOIUrl":"10.1038/s41437-025-00801-w","url":null,"abstract":"Inbreeding depression is the reduction in fitness of inbred individuals relative to their more outbred counterparts. Parasitism also reduces fitness and is a route by which inbreeding depression may operate, yet the complete pathway from inbreeding to parasitism to fitness has almost never been documented in the wild. We investigated parasite-mediated inbreeding depression in a wild population of a large mammal (red deer, Cervus elaphus), using high-quality individual-level data on fitness in juveniles and adult females, longitudinal infection data for three gastrointestinal helminth parasites, and genomic inbreeding coefficients. We found evidence for parasite-mediated inbreeding depression via strongyle nematodes in juvenile survival, independent of direct adverse effects of inbreeding on survival and indirect effects of inbreeding on survival via birth weight. Inbreeding also reduced fitness in reproductive adults by reducing overwinter survival. Our study reveals three independent pathways by which inbreeding depresses fitness and highlights the rarely-studied route of parasitism.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"134 10-11","pages":"637-644"},"PeriodicalIF":3.9,"publicationDate":"2025-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.comhttps://www.nature.com/articles/s41437-025-00801-w.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145205901","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"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 : 2025-09-30DOI: 10.1038/s41437-025-00799-1
Thomas Liehr, Sigrid Fuchs
{"title":"Unanswered questions when human karyotyping shows a supernumerary chromosome.","authors":"Thomas Liehr, Sigrid Fuchs","doi":"10.1038/s41437-025-00799-1","DOIUrl":"https://doi.org/10.1038/s41437-025-00799-1","url":null,"abstract":"","PeriodicalId":12991,"journal":{"name":"Heredity","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2025-09-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145199071","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Nutrition plays a central role in healthy living, however, extensive variability in individual responses to dietary interventions complicates our understanding of its effects. Here we present a comprehensive study utilizing the Drosophila Genetic Reference Panel (DGRP), investigating how genetic variation influences responses to diet and aging. We performed quantitative genetic analyses of the impact of reduced nutrient intake on lifespan, locomotor activity, dry weight, and heat knockdown time (HKDT) measured on the same individual flies. We found a significant decrease in lifespan for flies exposed to a restricted diet compared to those on a control diet. Similarly, a notable reduction in dry weight was observed in 7 and 16-day-old flies on the restricted diet compared to the control diet. In contrast, flies on the restricted diet exhibited higher locomotor activity. Additionally, HKDT was found to be age-dependent. Further, we detected significant genotype-by-diet interaction (GDI), genotype-by-age interaction (GAI) and genotype-by-age-by-diet interaction (GADI) for all traits. Thus, environmental factors play a crucial role in shaping trait variation at different ages and diets, and/or distinct genetic variation influences these traits at different ages and diets. Our genome-wide association study also identified a quantitative trait locus for age-dependent dietary response. The observed GDI and GAI indicate that susceptibility to environmental influences changes as organisms age. These findings could have significant implications for understanding the genetic mechanisms underlying dietary responses and aging in Drosophila melanogaster, which may inform future research on dietary recommendations and interventions aimed at promoting healthy aging in humans. The identification of associations between DNA sequence variation and age-dependent dietary responses opens new avenues for research into the genetic mechanisms underlying these interactions.
{"title":"The role of genetic variation in shaping phenotypic responses to diet in aging Drosophila melanogaster","authors":"Nikolaj Klausholt Bak, Trudy F. C. Mackay, Fabio Morgante, Kåre Lehmann Nielsen, Jeppe Lund Nielsen, Torsten Nygaard Kristensen, Palle Duun Rohde","doi":"10.1038/s41437-025-00797-3","DOIUrl":"10.1038/s41437-025-00797-3","url":null,"abstract":"Nutrition plays a central role in healthy living, however, extensive variability in individual responses to dietary interventions complicates our understanding of its effects. Here we present a comprehensive study utilizing the Drosophila Genetic Reference Panel (DGRP), investigating how genetic variation influences responses to diet and aging. We performed quantitative genetic analyses of the impact of reduced nutrient intake on lifespan, locomotor activity, dry weight, and heat knockdown time (HKDT) measured on the same individual flies. We found a significant decrease in lifespan for flies exposed to a restricted diet compared to those on a control diet. Similarly, a notable reduction in dry weight was observed in 7 and 16-day-old flies on the restricted diet compared to the control diet. In contrast, flies on the restricted diet exhibited higher locomotor activity. Additionally, HKDT was found to be age-dependent. Further, we detected significant genotype-by-diet interaction (GDI), genotype-by-age interaction (GAI) and genotype-by-age-by-diet interaction (GADI) for all traits. Thus, environmental factors play a crucial role in shaping trait variation at different ages and diets, and/or distinct genetic variation influences these traits at different ages and diets. Our genome-wide association study also identified a quantitative trait locus for age-dependent dietary response. The observed GDI and GAI indicate that susceptibility to environmental influences changes as organisms age. These findings could have significant implications for understanding the genetic mechanisms underlying dietary responses and aging in Drosophila melanogaster, which may inform future research on dietary recommendations and interventions aimed at promoting healthy aging in humans. The identification of associations between DNA sequence variation and age-dependent dietary responses opens new avenues for research into the genetic mechanisms underlying these interactions.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"134 10-11","pages":"611-623"},"PeriodicalIF":3.9,"publicationDate":"2025-09-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.comhttps://www.nature.com/articles/s41437-025-00797-3.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145137322","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"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 : 2025-09-23DOI: 10.1038/s41437-025-00788-4
David E. Ausband
Genetic diversity is an important driver affecting the health of wildlife populations. In cooperatively breeding species, human impacts and breeder turnover can affect genetic diversity in groups. We generally do not have strong inferences about how the genetic composition of a group changes through time as individuals are lost (e.g., die, emigrate) or adopted (e.g., immigrate). I wanted to know how breeder turnover, group size, and harvest affected the fluctuation of unique alleles in groups of gray wolves (Canis lupus) in Idaho, USA, during 2008–2020. Turnover of breeding males was strongly associated with allelic change in groups. Turnover of breeding females also had a strong association with allelic change in groups, but was not the most supported model. Harvest was strongly correlated with breeding female turnover but not breeding male turnover. Outside of breeding female turnover, harvest generally had little effect on allelic change in groups. Groups rarely adopted new individuals unless there was a breeding vacancy. I show that over time groups gain and lose alleles in roughly equal proportions, but there are episodic changes to alleles in groups as a function of breeding male turnover. These findings have implications for how we define and evaluate group persistence and breeder lineages in cooperative breeders. Such definitions have important implications for studying the evolution and maintenance of cooperative breeding. It may be beneficial to define characteristics and vital rates of groups based, at least in part, on their underlying genetics when such information can be obtained.
{"title":"Breeder turnover creates allelic variation in groups of gray wolves","authors":"David E. Ausband","doi":"10.1038/s41437-025-00788-4","DOIUrl":"10.1038/s41437-025-00788-4","url":null,"abstract":"Genetic diversity is an important driver affecting the health of wildlife populations. In cooperatively breeding species, human impacts and breeder turnover can affect genetic diversity in groups. We generally do not have strong inferences about how the genetic composition of a group changes through time as individuals are lost (e.g., die, emigrate) or adopted (e.g., immigrate). I wanted to know how breeder turnover, group size, and harvest affected the fluctuation of unique alleles in groups of gray wolves (Canis lupus) in Idaho, USA, during 2008–2020. Turnover of breeding males was strongly associated with allelic change in groups. Turnover of breeding females also had a strong association with allelic change in groups, but was not the most supported model. Harvest was strongly correlated with breeding female turnover but not breeding male turnover. Outside of breeding female turnover, harvest generally had little effect on allelic change in groups. Groups rarely adopted new individuals unless there was a breeding vacancy. I show that over time groups gain and lose alleles in roughly equal proportions, but there are episodic changes to alleles in groups as a function of breeding male turnover. These findings have implications for how we define and evaluate group persistence and breeder lineages in cooperative breeders. Such definitions have important implications for studying the evolution and maintenance of cooperative breeding. It may be beneficial to define characteristics and vital rates of groups based, at least in part, on their underlying genetics when such information can be obtained.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"134 10-11","pages":"577-583"},"PeriodicalIF":3.9,"publicationDate":"2025-09-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.comhttps://www.nature.com/articles/s41437-025-00788-4.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145130500","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"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 : 2025-09-18DOI: 10.1038/s41437-025-00795-5
Matilda Q. R. Pembury Smith, Laura Latkova, Rhonda R. Snook
The ecology of mating interactions determines a species’ mating system, yet whether environmental change can alter the mating system of a species remains unclear. Elevated temperatures can cause male sterility, prompting females to remate for fertility assurance. In monandrous systems, heat-induced male infertility poses a significant extinction risk, as females may mate exclusively with infertile males. A key question is whether male sterility could drive polyandry in a typically monandrous system. Here we address this by examining genetic variance underlying both male fertility resilience to heat stress and facultative polyandry, and assessing the fitness consequences of each mating system. We used isofemales lines of Drosophila subobscura, a monandrous species, exposing males to developmental heat stress. Male heat stress generated sterility and females mated to these males typically remated. While significant genetic variation in male fertility sensitivity and female remating emerged at moderate to high temperatures, we found little genetic variation in plasticity for polyandry. These results indicate evolutionary potential in both traits, but that a shift in mating system would arise through selection on genes associated with polyandry, rather than plasticity. Polyandry improved offspring production after initially mating to a sterile male, but did not fully restore reproductive output relative to fertile monandrous pairs, and mating with heat-stressed males increased female mortality. Heat stress also altered mating behaviour which could impact female mate choice. Together, these findings show that increasing temperatures may shape species’ mating systems and the interplay between thermal ecology and sexual selection under climate change.
{"title":"Facultative polyandry under heat stress and the evolutionary potential for climate-driven shifts in mating systems","authors":"Matilda Q. R. Pembury Smith, Laura Latkova, Rhonda R. Snook","doi":"10.1038/s41437-025-00795-5","DOIUrl":"10.1038/s41437-025-00795-5","url":null,"abstract":"The ecology of mating interactions determines a species’ mating system, yet whether environmental change can alter the mating system of a species remains unclear. Elevated temperatures can cause male sterility, prompting females to remate for fertility assurance. In monandrous systems, heat-induced male infertility poses a significant extinction risk, as females may mate exclusively with infertile males. A key question is whether male sterility could drive polyandry in a typically monandrous system. Here we address this by examining genetic variance underlying both male fertility resilience to heat stress and facultative polyandry, and assessing the fitness consequences of each mating system. We used isofemales lines of Drosophila subobscura, a monandrous species, exposing males to developmental heat stress. Male heat stress generated sterility and females mated to these males typically remated. While significant genetic variation in male fertility sensitivity and female remating emerged at moderate to high temperatures, we found little genetic variation in plasticity for polyandry. These results indicate evolutionary potential in both traits, but that a shift in mating system would arise through selection on genes associated with polyandry, rather than plasticity. Polyandry improved offspring production after initially mating to a sterile male, but did not fully restore reproductive output relative to fertile monandrous pairs, and mating with heat-stressed males increased female mortality. Heat stress also altered mating behaviour which could impact female mate choice. Together, these findings show that increasing temperatures may shape species’ mating systems and the interplay between thermal ecology and sexual selection under climate change.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"134 10-11","pages":"596-604"},"PeriodicalIF":3.9,"publicationDate":"2025-09-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.comhttps://www.nature.com/articles/s41437-025-00795-5.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145080446","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"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 : 2025-09-16DOI: 10.1038/s41437-025-00796-4
Sai Wei, Zhibing Li, Xin Lu
While extra-pair mating prevails among socially monogamous birds, it does not occur in all individuals within a population. Then, what underlies this variability? A poorly explored mechanism is the genetic contribution to the behavioral trait, especially for cooperatively breeding species where promiscuity may potentially conflict with the acquisition of indirect benefits to altruistic helpers. We addressed the gap through a quantitative genetic approach with 8 years of data from an individually marked population of Tibetan ground tits (Pseudopodoces humilis). Extra-pair mating was observed in 33.2% of nests, and cooperative breeding occurred in 39.5% of nests. Animal models demonstrated no significant genetic component contributing to the variance in extra-pair mating both during a specific year and over an individual’s lifetime. Consequently, the heritabilities were not significantly different from zero. The lack of heritable variation in extra-pair mating can be accounted for by Fisher’s fundamental theorem of natural selection, which suggests that genotypes associated with this behavior facilitating reproductive success should have become widespread within the population. Furthermore, the fitness benefits derived from promiscuity were greater for breeders than those from receiving help; for helpers, the fitness benefits from extra-pair mating outweighed the indirect genetic benefits obtained from providing help. This may explain why extra-pair mating and cooperative breeding can coexist in the same population. Our findings imply that individual variation in performing extra-pair mating behavior is more likely to be influenced by environmental factors.
{"title":"No evidence for heritability of extra-pair mating behavior in a cooperatively breeding bird","authors":"Sai Wei, Zhibing Li, Xin Lu","doi":"10.1038/s41437-025-00796-4","DOIUrl":"10.1038/s41437-025-00796-4","url":null,"abstract":"While extra-pair mating prevails among socially monogamous birds, it does not occur in all individuals within a population. Then, what underlies this variability? A poorly explored mechanism is the genetic contribution to the behavioral trait, especially for cooperatively breeding species where promiscuity may potentially conflict with the acquisition of indirect benefits to altruistic helpers. We addressed the gap through a quantitative genetic approach with 8 years of data from an individually marked population of Tibetan ground tits (Pseudopodoces humilis). Extra-pair mating was observed in 33.2% of nests, and cooperative breeding occurred in 39.5% of nests. Animal models demonstrated no significant genetic component contributing to the variance in extra-pair mating both during a specific year and over an individual’s lifetime. Consequently, the heritabilities were not significantly different from zero. The lack of heritable variation in extra-pair mating can be accounted for by Fisher’s fundamental theorem of natural selection, which suggests that genotypes associated with this behavior facilitating reproductive success should have become widespread within the population. Furthermore, the fitness benefits derived from promiscuity were greater for breeders than those from receiving help; for helpers, the fitness benefits from extra-pair mating outweighed the indirect genetic benefits obtained from providing help. This may explain why extra-pair mating and cooperative breeding can coexist in the same population. Our findings imply that individual variation in performing extra-pair mating behavior is more likely to be influenced by environmental factors.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"134 10-11","pages":"605-610"},"PeriodicalIF":3.9,"publicationDate":"2025-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145075213","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-09-08DOI: 10.1038/s41437-025-00794-6
Xuyue Yang, Kalle Tunström, Tanja Slotte, Christopher W. Wheat, Peter A. Hambäck
Parasitoid wasps are major causes of mortality of many species, making host immune defences a common target of adaptive evolution, though such targets outside model species are poorly understood. In this study, we used two tests of positive selection to compare across three closely related Galerucella leaf beetles that show substantial differences in their phenotypic response to the shared parasitoid wasp Asecodes parviclava, their main natural enemy. Using a codon-based test, which detects excess amino acid fixations per locus along each species’ lineage, we found more evidence of positive selection on parasitoid-relevant immune genes in the species with the strongest immunocompetence (G. pusilla) compared with the species having weaker immunocompetence (G. tenella and G. calmariensis). Moreover, genes coding for the early phases in the immune response cascade were predominantly among the positively selected immune genes, providing targets for future functional genomic study to pin-point connections between genotypic and phenotypic differences in defences towards a parasitoid wasp. In contrast, genome-wide analyses of the haplotype frequency spectrum, which quantify selection over recent evolutionary time scales, revealed similar signatures of positive selection on immune genes across species. These results advance the field of host-parasitoid dynamics by providing novel insights into the tempo and mode of insect host evolutionary dynamics, and offering a framework for making genotype to phenotype connections for immunocompetence phenotypes.
{"title":"Lineage-specific targets of positive selection in three leaf beetles correspond with defence capacity against their shared parasitoid wasp","authors":"Xuyue Yang, Kalle Tunström, Tanja Slotte, Christopher W. Wheat, Peter A. Hambäck","doi":"10.1038/s41437-025-00794-6","DOIUrl":"10.1038/s41437-025-00794-6","url":null,"abstract":"Parasitoid wasps are major causes of mortality of many species, making host immune defences a common target of adaptive evolution, though such targets outside model species are poorly understood. In this study, we used two tests of positive selection to compare across three closely related Galerucella leaf beetles that show substantial differences in their phenotypic response to the shared parasitoid wasp Asecodes parviclava, their main natural enemy. Using a codon-based test, which detects excess amino acid fixations per locus along each species’ lineage, we found more evidence of positive selection on parasitoid-relevant immune genes in the species with the strongest immunocompetence (G. pusilla) compared with the species having weaker immunocompetence (G. tenella and G. calmariensis). Moreover, genes coding for the early phases in the immune response cascade were predominantly among the positively selected immune genes, providing targets for future functional genomic study to pin-point connections between genotypic and phenotypic differences in defences towards a parasitoid wasp. In contrast, genome-wide analyses of the haplotype frequency spectrum, which quantify selection over recent evolutionary time scales, revealed similar signatures of positive selection on immune genes across species. These results advance the field of host-parasitoid dynamics by providing novel insights into the tempo and mode of insect host evolutionary dynamics, and offering a framework for making genotype to phenotype connections for immunocompetence phenotypes.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"134 9","pages":"567-575"},"PeriodicalIF":3.9,"publicationDate":"2025-09-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.comhttps://www.nature.com/articles/s41437-025-00794-6.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145023146","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"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 : 2025-08-25DOI: 10.1038/s41437-025-00789-3
Yuwei Cui, Leonard Nunney
Karyotype variation within Pacific kangaroo rat Dipodomys agilis motivated its division in 1997 into the agile kangaroo rat (AKR, D. agilis, 2N = 62) in the north of its range in California, and Dulzura kangaroo rat (DKR, D. simulans, 2N = 60) to the south, with a suspected sympatric zone south of the San Gabriel and San Bernardino Mountains. This division was supported by our whole genome sequencing that sampled a ~120 km transect from north of the mountains to SW Riverside County. The taxa showed marked genetic differentiation, with no evidence of hybridization or sympatry. AKR was found at the southern edge of the mountains, precluding the mountain barrier driving isolation, suggesting ecological separation linked to habitat differences between the mountains and the arid area to the south. Adding four additional Dipodomys species, we estimated genetic divergence times in the genus back to ∼3.5 mya. AKR and DKR diverged from D. stephensi ∼1.7 mya, and from each other ∼0.5 mya, when their joint effective population size (Ne) was ~100,000. After separation, DKR’s Ne declined to ~20,000, while AKR’s was little changed. More recently their Ne converged at ~50,000. Runs of homozygosity were longer in AKR, indicating a smaller neighborhood size, which may have promoted the karyotype change; however, nucleotide diversity was higher in AKR, but both had levels typical for rodents, indicating neither experienced recent bottlenecks. These patterns provide a baseline for any future conservation efforts. More generally, this study shows how a detailed genomic study can resolve taxonomic and demographic questions among morphologically indistinguishable taxa.
太平洋袋鼠鼠（Dipodomys agilis）的核型变异促使其于1997年在其加利福尼亚活动范围的北部分裂为敏捷袋鼠鼠（AKR， D. agilis, 2N = 62），在其南部分裂为Dulzura袋鼠鼠（DKR， D. simulans, 2N = 60），在圣加布里埃尔山脉和圣贝纳迪诺山脉以南疑似同属区。我们的全基因组测序支持了这一划分，我们对从山区北部到河滨县西南部约120公里的样带进行了采样。该分类群表现出明显的遗传分化，没有杂交或同属的证据。AKR出现在山脉的南部边缘，排除了山脉屏障导致的隔离，表明山脉与南部干旱地区之间的栖息地差异与生态分离有关。再加上另外四个双足属物种，我们估计该属的遗传分化时间可追溯到3.5亿年前。当AKR和DKR的联合有效种群大小（Ne）为~100,000时，它们与斯蒂芬氏笛虫的分化时间为~ 1.7万年，彼此分化时间为~ 0.5万年。分离后，DKR的Ne下降到~ 20000，而AKR的Ne变化不大。最近，它们的Ne收敛到~50,000。AKR的纯合序列较长，表明其邻域较小，这可能促进了核型的变化；然而，AKR的核苷酸多样性更高，但两者都具有啮齿类动物的典型水平，表明两者都没有经历最近的瓶颈。这些模式为未来的保护工作提供了一个基准。更一般地说，这项研究显示了详细的基因组研究如何解决形态上难以区分的分类群之间的分类学和人口学问题。
{"title":"Genomic analysis of differentiation and demography of the formerly conspecific agile (Dipodomys agilis) and Dulzura (D. simulans) kangaroo rats","authors":"Yuwei Cui, Leonard Nunney","doi":"10.1038/s41437-025-00789-3","DOIUrl":"10.1038/s41437-025-00789-3","url":null,"abstract":"Karyotype variation within Pacific kangaroo rat Dipodomys agilis motivated its division in 1997 into the agile kangaroo rat (AKR, D. agilis, 2N = 62) in the north of its range in California, and Dulzura kangaroo rat (DKR, D. simulans, 2N = 60) to the south, with a suspected sympatric zone south of the San Gabriel and San Bernardino Mountains. This division was supported by our whole genome sequencing that sampled a ~120 km transect from north of the mountains to SW Riverside County. The taxa showed marked genetic differentiation, with no evidence of hybridization or sympatry. AKR was found at the southern edge of the mountains, precluding the mountain barrier driving isolation, suggesting ecological separation linked to habitat differences between the mountains and the arid area to the south. Adding four additional Dipodomys species, we estimated genetic divergence times in the genus back to ∼3.5 mya. AKR and DKR diverged from D. stephensi ∼1.7 mya, and from each other ∼0.5 mya, when their joint effective population size (Ne) was ~100,000. After separation, DKR’s Ne declined to ~20,000, while AKR’s was little changed. More recently their Ne converged at ~50,000. Runs of homozygosity were longer in AKR, indicating a smaller neighborhood size, which may have promoted the karyotype change; however, nucleotide diversity was higher in AKR, but both had levels typical for rodents, indicating neither experienced recent bottlenecks. These patterns provide a baseline for any future conservation efforts. More generally, this study shows how a detailed genomic study can resolve taxonomic and demographic questions among morphologically indistinguishable taxa.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"134 9","pages":"519-528"},"PeriodicalIF":3.9,"publicationDate":"2025-08-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.comhttps://www.nature.com/articles/s41437-025-00789-3.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144952002","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"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 : 2025-08-24DOI: 10.1038/s41437-025-00790-w
José M. Rico-Porras, Pablo Mora, Ana E. Gasparotto, Vanessa B. Bardella, Teresa Palomeque, Pedro Lorite, Diogo C. Cabral-de-Mello
Repetitive DNA sequences are ubiquitous in eukaryotic genomes, significantly influencing their structure, function, and evolution. They can facilitate genomic rearrangements, contributing to chromosomal and genomic diversity. Chrysomelidae (Coleoptera) beetles are known for their highly diverse karyotypes and heterochromatin distribution. In this study, we advanced the understanding of the intricate relationship between satellite DNA-like sequences (named here solely as satDNA) and genome organization/reshuffling using three species of Eumolpinae chrysomelids. We investigated the satellitomes of three species with divergent karyotypes that had undergone independent chromosomal fusions: Colaspis laeta (2n = 22, Xyp), with a conserved karyotype; Endocephalus bigatus (2n = 10, neo-XY); and Iphimeis dives (2n = 14, neo-XY). Our comparative analysis revealed highly divergent patterns of satDNA origin, organization, and evolution. In species with reduced chromosome numbers and neo-sex chromosomes, we observed a high abundance of transposable element-related (TE-related) satDNAs. In Colaspis laeta, the sex chromosomes (Xyp) showed an advanced level of differentiation. However, in the species with a reduction in diploid number, such a level of differential enrichment of repetitive DNAs was not observed in the sex chromosomes, indicating an early stage of differentiation. Our findings support the hypothesis that chromosomal rearrangements and reorganization of repetitive DNA sequences are connected, with extensive reshuffling observed in species with reduced diploid numbers. Moreover, the data reinforce the involvement of TEs in satDNA origin, which could spread widely throughout the genome, including euchromatic areas. This study provides new insights into the evolutionary dynamics of repetitive DNAs in non-model species, emphasizing the impact of chromosomal rearrangements on genome architecture and evolution.
{"title":"Expansion of satellite DNAs derived from transposable elements in beetles with reduced diploid numbers","authors":"José M. Rico-Porras, Pablo Mora, Ana E. Gasparotto, Vanessa B. Bardella, Teresa Palomeque, Pedro Lorite, Diogo C. Cabral-de-Mello","doi":"10.1038/s41437-025-00790-w","DOIUrl":"10.1038/s41437-025-00790-w","url":null,"abstract":"Repetitive DNA sequences are ubiquitous in eukaryotic genomes, significantly influencing their structure, function, and evolution. They can facilitate genomic rearrangements, contributing to chromosomal and genomic diversity. Chrysomelidae (Coleoptera) beetles are known for their highly diverse karyotypes and heterochromatin distribution. In this study, we advanced the understanding of the intricate relationship between satellite DNA-like sequences (named here solely as satDNA) and genome organization/reshuffling using three species of Eumolpinae chrysomelids. We investigated the satellitomes of three species with divergent karyotypes that had undergone independent chromosomal fusions: Colaspis laeta (2n = 22, Xyp), with a conserved karyotype; Endocephalus bigatus (2n = 10, neo-XY); and Iphimeis dives (2n = 14, neo-XY). Our comparative analysis revealed highly divergent patterns of satDNA origin, organization, and evolution. In species with reduced chromosome numbers and neo-sex chromosomes, we observed a high abundance of transposable element-related (TE-related) satDNAs. In Colaspis laeta, the sex chromosomes (Xyp) showed an advanced level of differentiation. However, in the species with a reduction in diploid number, such a level of differential enrichment of repetitive DNAs was not observed in the sex chromosomes, indicating an early stage of differentiation. Our findings support the hypothesis that chromosomal rearrangements and reorganization of repetitive DNA sequences are connected, with extensive reshuffling observed in species with reduced diploid numbers. Moreover, the data reinforce the involvement of TEs in satDNA origin, which could spread widely throughout the genome, including euchromatic areas. This study provides new insights into the evolutionary dynamics of repetitive DNAs in non-model species, emphasizing the impact of chromosomal rearrangements on genome architecture and evolution.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":"134 9","pages":"529-541"},"PeriodicalIF":3.9,"publicationDate":"2025-08-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144951995","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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