Heritable Variation Research Articles

Estimates of microbiome heritability across hosts.

Microbiomes contribute to variation in many plant and animal traits, suggesting that microbiome-mediated traits could evolve through selection on the host. However, for such evolution to occur, microbiomes must exhibit sufficient heritability to contribute to host adaptation. Previous work has attempted to estimate the heritability of a variety of microbiome attributes. Here we show that most published estimates are limited to vertebrate and plant hosts, but significant heritability of microbiome attributes has been frequently reported. This indicates that microbiomes could evolve in response to host-level selection, but studies across a wider range of hosts are necessary before general conclusions can be made. We suggest future studies focus on standardizing heritability measurements for the purpose of meta-analyses and investigate the role of the environment in contributing to heritable microbiome variation. This could have important implications for the use of microbiomes in conservation, agriculture and medicine.

Human culture is uniquely open-ended rather than uniquely cumulative.

Theories of how humans came to be so ecologically dominant increasingly centre on the adaptive abilities of human culture and its capacity for cumulative change and high-fidelity transmission. Here we revisit this hypothesis by comparing human culture with animal cultures and cases of epigenetic inheritance and parental effects. We first conclude that cumulative change and high transmission fidelity are not unique to human culture as previously thought, and so they are unlikely to explain its adaptive qualities. We then evaluate the evidence for seven alternative explanations: the inheritance of acquired characters, the pathways of inheritance, the non-random generation of variation, the scope of heritable variation, effects on organismal fitness, effects on genetic fitness and effects on evolutionary dynamics. From these, we identify the open-ended scope of human cultural variation as a key, but generally neglected, phenomenon. We end by articulating a hypothesis for the cognitive basis of this open-endedness.

Genetic analysis of maize crude fat content by multi-locus genome-wide association study

Crude fat is an important nutritional component of maize kernels. However, the genetic mechanisms underlying crude fat content in maize kernels remain elusive. Previous studies used single-model genome-wide association studies (GWAS) with limited population sizes, which can result in false positives of loci and hinder the identification of functional genes. Therefore, this study used a population consisting of 495 maize inbred lines, combined with 1.25 million single nucleotide polymorphisms (SNPs), and implemented GWAS using six models to identify quantitative trait nucleotides (QTNs) controlling crude fat content and to mine key genes. The results revealed a wide variation in crude fat content (0.62–16.03%) and broad-sense heritability (96.23%). In total, 744 significant QTNs were detected, with 147 co-located across different models, environments, and methods. Based on the 147 co-located QTNs, candidate genes were searched at 50 kb up- and downstream intervals of each QTN. We finally screened eight candidate genes (GRMZM2G169089, GRMZM2G117935, GRMZM2G002075, GRMZM2G368838, GRMZM2G058496, GRMZM2G090669, GRMZM2G001241, and GRMZM2G333454) related to crude fat content that exhibited high expression levels during kernel development in maize inbred line B73. Notably, GRMZM2G169089, GRMZM2G117935, GRMZM2G002075, and GRMZM2G368838 are involved in the linoleic acid metabolic pathway, oil metabolism, kernel growth, and development in maize. Furthermore, co-expression network analysis revealed that the eight candidate genes exhibited strong correlations with 30 known genes. Proteins encoded by candidate genes interact with various other proteins and play an important role in oil content and oleic acid metabolism in maize kernels. The best haplotypes of candidate genes might increase crude fat content without decreasing maize yield. These results broaden the understanding of the genetic mechanism of crude fat content and facilitate marker-assisted selection for high-crude fat breeding programs for maize.

Genetic Variation in Trophic Avoidance Behaviour Shows Fruit Flies are Generally Attracted to Bacterial Substrates.

Pathogen avoidance behaviours are often assumed to be an adaptive host defence. However, there is limited experimental data on heritable, intrapopulation phenotypic variation for avoidance, a strong prerequisite for adaptive responses to selection. We investigated trophic pathogen avoidance in 122 inbred Drosophila melanogaster lines, and in a derived outbred population. Using the FlyPAD system, we tracked the feeding choice that flies made between substrates that were either clean or contained a bacterial pathogen. We uncovered significant, but weakly heritable variation in the preference index amongst fly lines. However, instead of avoidance, most lines demonstrated a preference for substrates containing several bacterial pathogens, showing avoidance only for extremely high bacterial concentrations. Bacterial preference was not associated with susceptibility to infection and was retained in flies with disrupted immune signalling. Phenotype-genotype association analysis indicated several novel genes (CG2321, CG2006, and ptp99A) associated with increased preference for the bacterial substrate, while the amino-acid transporter sobremesa was associated with greater aversion. Given the known fitness benefits of consuming high-protein diets, our results suggest that bacterial attraction may instead reflect a dietary preference for protein over carbohydrate. More work quantifying intrapopulation variation in avoidance behaviours is needed to fully assess its importance in host-pathogen evolutionary ecology.

Physiological phenotyping of transpiration response to vapour pressure deficit in wheat

BackgroundPrecision phenotyping of short-term transpiration response to environmental conditions and transpiration patterns throughout wheat development enables a better understanding of specific trait compositions that lead to improved transpiration efficiency. Transpiration and related traits were evaluated in a set of 79 winter wheat lines using the custom-built “DroughtSpotter XXL” facility. The 120 l plant growth containers implemented in this phenotyping platform enable gravimetric quantification of water use in real-time under semi-controlled, yet field-like conditions across the entire crop life cycle.ResultsThe resulting high-resolution data enabled identification of significant developmental stage-specific variation for genotype rankings in transpiration efficiency. In addition, for all examined genotypes we identified the genotype-specific breakpoint in transpiration in response to increasing vapour pressure deficit, with breakpoints ranging between 2.75 and 4.1 kPa.ConclusionContinuous monitoring of transpiration efficiency and diurnal transpiration patterns enables identification of hidden, heritable genotypic variation for transpiration traits relevant for wheat under drought stress. Since the unique experimental setup mimics field-like growth conditions, the results of this study have good transferability to field conditions.

A "poly-matter network" conception of biological inheritance.

Here we intend to shift the "DNA- and information-centric" conception of biological inheritance, with the accompanying exclusion of any non-DNA matter, to a "poly-matter network" framework which, in addition to DNA, considers the action of other cellular membranous constituents. These cellular structures, in particular organelles and plasma membranes, express "landscapes" of specific topologies at their surfaces, which may become altered in response to certain environmental factors. These so-called "membranous environmental landscapes" (MELs), which replicate by self-organization / autopoiesis rather than self-assembly, are transferred from donor to acceptor cells by various - vesicular and non-vesicular - mechanisms and exert novel features in the acceptor cells. The "DNA-centric" conception may be certainly explanatorily sufficient for the transfer of heritable phenotype variation to acceptor cells following the copying of DNA in donor cells and thereby for the phenomenon of biological inheritance of traits. However, it is not causally sufficient. With the observation of phenotype variation, as initially manifested during bacterial transformation, the impact of environmental factors, such as nutrition and stress, in the differential regulation of gene expression has been widely accepted and resulted in intense efforts to resolve the underlying epigenetic mechanisms. However, these are explained under a conceptual frame where the DNA (and associated proteins) are the only matter of inheritance. In contrast, it is our argumentation that inheritance can only be adequately understood as the transfer of DNA in concert with non-DNA matter in a "poly-matter network" conception. The adequate inclusion of the transfer of non-DNA matter is still a desideratum of future genetic research, which may pave the way for the experimental elucidation not only of how DNA and membrane matter act in concert to enable the inheritance of innate traits, but also whether they interact for that of acquired biological traits. Moreover, the "poly-matter network" conception may open new perspectives for an understanding of the pathogenesis of "common complex" diseases.

Indirect genetic effects increase the heritable variation available to selection and are largest for behaviors: a meta-analysis

Indirect genetic effects increase the heritable variation available to selection and are largest for behaviors: a meta-analysis

Multitemporal UAV study of phenolic compounds in slash pine canopies

Phenolic compounds (PC) are important secondary metabolites in plants, playing a crucial role in plant defense mechanisms against pathogens and other plants. Monitoring PC levels is important for understanding tree stress and implementing effective breeding programs. However, traditional methods for monitoring PC are time-consuming, prone to altering the phenolic composition, and mostly applicable only on a small scale. In this study, we evaluated the performance of Unoccupied Aerial Vehicles (UAV) multispectral imaging in estimating the canopy phenolic content in slash pine over an 11-month period in 2021 and a seven-month period in 2022. Three machine learning models including Partial least squares regression (PLSR), Random forest (RF) and Support Vector Machine (SVM) were compared to determine the optimal predictive model for canopy PC. The RF model provided the best predictive results, with R2 values of 0.82 for the validation set and 0.94 for the calibration set. Additionally, the study assesses the heritable variation in canopy PC over time, with the monthly heritability (h2) of PC ranging from 0 to 0.26 in 2021 and from 0 to 0.35 in 2022; The highest h2 levels were observed in July and September 2021and July 2022. The findings demonstrate significant genetic control over the variation of PC. Furthermore, we observed higher breeding values and genetic gains in July and November, which further supports the strong correlation between PC and environmental factors such as temperature and light intensity. To the best of our knowledge, this is the first study to employ time-series UAV multispectral imaging to predict secondary metabolites in pine trees and estimate their genetic variation over time. As a proof of concept, these findings provide more reliable information for tree breeding programs, ultimately enhancing their overall performance.

Research Progress into the Biological Functions of IFITM3.

Interferon-induced transmembrane proteins (IFITMs) are upregulated by interferons. They are not only highly conserved in evolution but also structurally consistent and have almost identical structural domains and functional domains. They are all transmembrane proteins and have multiple heritable variations in genes. The IFITM protein family is closely related to a variety of biological functions, including antiviral immunity, tumor formation, bone metabolism, cell adhesion, differentiation, and intracellular signal transduction. The progress of the research on its structure and related functions, as represented by IFITM3, is reviewed.

Performance and Stability for Grain Yield and Its Components of Some Rice Cultivars under Various Environments

Refine current agricultural practices considering environmental changes are crucial for finding tolerant rice varieties that can meet the demands of human consumption. To this end, stability analysis assesses a crop genotype’s ability to adapt to various conditions. Therefore, the objective of this study was to (1) examine the interaction between rice genotypes and environmental conditions; (2) evaluate the stability of twelve rice genotypes using various stability methods; (3) identify representative environments for multi-environment testing; and (4) determine superior genotypes for specific environments. The evaluated rice cultivars were Sakha 101, Sakha 104, Sakha 105, Sakha 106, Sakha 107, Sakha 108, Giza 177, Giza 178, Giza 179, Giza 182, Egyptian Yasmine, and Sakha super 300. The experiment followed a strip-plot design, with three replications. The findings revealed significant differences among the rice varieties across various environments for the majority of the assessed characteristics. The joint regression analysis of variance demonstrated highly significant differences among rice cultivars for all the studied traits in terms of genotype-by-environment interaction (G × E). The statistical significance of the interaction between genetic and environmental factors was evident for all variables demonstrating heritable variation among the rice cultivars, specifically Sakha 108, Sakha 104, Giza 177, and Giza 178, concerning grain yield per feddan. These rice cultivars exhibited stability parameters that were not significantly different from unity for the regression coefficient (bi) and from zero for the deviations from regression (S2di) for those traits. Overall, stability criteria are essential for ensuring reliable rice production, meeting human consumption, advancing genetic improvement, and promoting environmental sustainability in agriculture.

A new perspective on tumor progression: Evolution via selection for function.

Tumorigenesis is commonly attributed to Darwinian processes involving natural selection among cells and groups of cells. However, progressing tumors are those that also achieve an appropriate group phenotypic composition (GPC). Yet, the selective processes acting on tumor GPCs are distinct from that associated with classical Darwinian evolution (i.e. natural selection based on differential reproductive success) as tumors are not genuine evolutionary individuals and do not exhibit heritable variation in fitness. This complex evolutionary scenario is analogous to the recently proposed concept of 'selection for function' invoked for the evolution of both living and non-living systems. Therefore, we argue that it is inaccurate to assert that Darwinian processes alone account for all the aspects characterizing tumorigenesis and cancer progression; rather, by producing the genetic and phenotypic diversity required for creating novel GPCs, these processes fuel the evolutionary success of tumors that is dependent on selection for function at the tumor level.

Use of Phenomics in the Selection of UAV-Based Vegetation Indices and Prediction of Agronomic Traits in Soybean Subjected to Flooding

Flooding is a frequent environmental stress that reduces soybean growth and grain yield in many producing areas in the world, such as the United States, Southeast Asia, and Southern Brazil. In these regions, soybean is frequently cultivated in lowland areas in crop rotation with rice, which provides numerous technical, economic, and environmental benefits. In this context, the identification of the most important spectral variables for the selection of more flooding-tolerant soybean genotypes is a primary demand within plant phenomics, with faster and more reliable results enabled using multispectral sensors mounted on unmanned aerial vehicles (UAVs). Accordingly, this research aimed to identify the optimal UAV-based multispectral vegetation indices for characterizing the response of soybean genotypes subjected to flooding and to test the best linear model fit in predicting tolerance scores, relative maturity group, biomass, and grain yield based on phenomics analysis. Forty-eight soybean cultivars were sown in two environments (flooded and non-flooded). Ground evaluations and UAV-image acquisition were conducted at 13, 38, and 69 days after flooding and at grain harvest, corresponding to the phenological stages V8, R1, R3, and R8, respectively. Data were subjected to variance component analysis and genetic parameters were estimated, with stepwise regression applied for each agronomic variable of interest. Our results showed that vegetation indices behave differently in their suitability for more tolerant genotype selection. Using this approach, phenomics analysis efficiently identified indices with high heritability, accuracy, and genetic variation (>80%), as observed for MSAVI, NDVI, OSAVI, SAVI, VEG, MGRVI, EVI2, NDRE, GRVI, BNDVI, and RGB index. Additionally, variables predicted based on estimated genetic data via phenomics had determination coefficients above 0.90, enabling the reduction in the number of important variables within the linear model.

The Dominance of Coinfecting Parasites' Indirect Genetic Effects on Host Traits.

AbstractIndirect genetic effects (IGEs) exist when there is heritable variation in one organism's ability to alter a second organism's traits. For example, parasites have antigens that can induce a host immune response, as well as disparate strategies to evade or suppress host immunity; among-parasite genetic variation in these antigens generates among-host variation in immune traits. Here, we experimentally show that the cestode parasite Schistocephalus solidus exerts an IGE on an immune trait (peritoneal fibrosis) in its threespine stickleback host: stickleback developed strong fibrosis after exposure to some parasite genotypes but not others. A complication arises during coinfection, when two or more parasite genotypes may impose conflicting IGEs on the same host trait. What parasite-controlled trait will the host express? Will the host trait reflect the more immune-stimulatory parasite genotype or the more immune-evasive genotype? These alternatives can be quantified by estimating the dominance coefficient, as if a coinfected host were a heterozygote. We experimentally estimated the dominance of S. solidus IGEs by coinjecting antigens from different parasite genotypes. Contrary to our a priori hypotheses, coinjected antigens induced an overdominant effect, stronger than either parasite's antigens alone. We present a mathematical model showing that the value of this IGE dominance is biologically important, affecting the evolutionary dynamics of parasites in a density- and frequency-dependent manner. The model indicates that overdominance would be detrimental to immigrants when resident prevalence is high. This combination of experimental data and modeling provides an example of a parasite IGE on host traits and the evolutionary significance of IGE dominance.

Thermal tolerance traits of individual corals are widely distributed across the Great Barrier Reef.

Adaptation of reef-building corals to global warming depends upon standing heritable variation in tolerance traits upon which selection can act. Yet limited knowledge exists on heat-tolerance variation among conspecific individuals separated by metres to hundreds of kilometres. Here, we performed standardized acute heat-stress assays to quantify the thermal tolerance traits of 709 colonies of Acropora spathulata from 13 reefs spanning 1060 km (9.5° latitude) of the Great Barrier Reef. Thermal thresholds for photochemical efficiency and chlorophyll retention varied considerably among individual colonies both among reefs (approximately 6°C) and within reefs (approximately 3°C). Although tolerance rankings of colonies varied between traits, the most heat-tolerant corals (i.e. top 25% of each trait) were found at virtually all reefs, indicating widespread phenotypic variation. Reef-scale environmental predictors explained 12-62% of trait variation. Corals exposed to high thermal averages and recent thermal stress exhibited the greatest photochemical performance, probably reflecting local adaptation and stress pre-acclimatization, and the lowest chlorophyll retention suggesting stress pre-sensitization. Importantly, heat tolerance relative to local summer temperatures was the greatest on higher latitude reefs suggestive of higher adaptive potential. These results can be used to identify naturally tolerant coral populations and individuals for conservation and restoration applications.

Heritable intraspecific variation among prey in size and movement interact to shape predation risk and potential natural selection

Abstract Predator and prey traits are important determinants of the outcomes of trophic interactions. In turn, the outcomes of trophic interactions shape predator and prey trait evolution. How species' traits respond to selection from trophic interactions depends crucially on whether and how heritable species' traits are and their genetic correlations. Of the many traits influencing the outcomes of trophic interactions, body size and movement traits have emerged as key traits. Yet, how these traits shape and are shaped by trophic interactions is unclear, as few studies have simultaneously measured the impacts of these traits on the outcomes of trophic interactions, their heritability, and their correlations within the same system. We used outcrossed lines of the ciliate protist Paramecium caudatum from natural populations to examine variation in morphology and movement behaviour, the heritability of that variation, and its effects on Paramecium susceptibility to predation by the copepod Macrocyclops albidus. We found that the Paramecium lines exhibited heritable variation in body size and movement traits. In contrast to expectations from allometric relationships, body size and movement speed showed little covariance among clonal lines. The proportion of Paramecium consumed by copepods was positively associated with Paramecium body size and velocity but with an interaction such that greater velocities led to greater predation risk for large body‐sized paramecia but did not alter predation risk for smaller paramecia. The proportion of paramecia consumed was not related to copepod body size. These patterns of predation risk and heritable trait variation in paramecia suggest that copepod predation may act as a selective force operating independently on movement and body size and generating the strongest selection against large, high‐velocity paramecia. Our results illustrate how ecology and genetics can shape potential natural selection on prey traits through the outcomes of trophic interactions. Further simultaneous measures of predation outcomes, traits, and their quantitative genetics will provide insights into the evolutionary ecology of species interactions and their eco‐evolutionary consequences. Read the free Plain Language Summary for this article on the Journal blog.

Voluntary nicotine consumption and reward in a subset of diversity outbred founder strains.

Nicotine is largely responsible for the initiation and maintenance of tobacco dependence and contributes to a global health problem. This study characterizes nicotine oral consumption and preference in male and female mice of several Diversity Outbred (DO) founder strains: C57BL/6J, A/J, 129S1/SvImJ, PWK/PhJ, NOD/ShiLtJ, and CAST/EiJ. It assesses the impact of nicotine concentration on intake and preference, the potential interaction of strain with sex, and estimates the degree of heritable variation in nicotine consumption. Two-bottle choice oral self-administration paradigm was used to assess nicotine intake, nicotine preference, and total fluid intake in male and female mice of each strain in a concentration-response manner. A conditioned place preference (CPP) test was performed to evaluate the rewarding and aversive effects of nicotine in certain strains after systemic administration of the drug. The highest nicotine-consuming strain was found to be 129S1/SvlmJ, and the lowest nicotine-consuming strain was A/J. Strain differences in nicotine intake were not due to differences in bitter and sweet tastes as shown in the saccharine and quinine two-bottle choice tests. A/J strain showed no significant CPP for nicotine while the 129S1/SvImJ strain showed a significant CPP for nicotine and a higher preference when compared to the C57BL/6J strain. Heritability estimates of nicotine intake were sex dependent and concentration dependent. Data support that nicotine consumption patterns are heritable with an influence of genotype in a voluntary oral self-administration paradigm. Results pave the way for future studies with the highly recombinant DO mice that might lead to the identification of novel genetic loci and genes influencing nicotine consumption.

Climatic variation allows montane willows to escape an adaptive trade-off.

Adaptive responses to climate change, based on heritable variation in stress tolerance, may be important for plant population persistence. It is unclear which populations will mount the strongest future adaptive responses. It may be fruitful to identify populations that have escaped trade-offs among performance traits, which can hinder adaptation. Barring strong genetic constraints, the extent of trade-offs may depend on spatial relationships among climate variables shaping different traits. Here, we test for climate-driven ecotypic variation and trade-offs among drought and freezing sensitivity, and growth, for Lemmon's willow (Salix lemmonii) in a common garden study of 90 genotypes from 38 sites in the Sierra Nevada, USA. Salix lemmonii exhibits ecotypic variation in leaf turgor loss point, a measure of drought sensitivity, from -0.95 to -0.74 MPa along a gradient of spring snowpack. We also find variation in spring freezing sensitivity with minimum May temperature. However, we find no trade-off, as the climatic gradients shaping these traits are spatially uncorrelated in our study region, despite being negatively correlated across the Sierra Nevada. Species may escape adaptive trade-offs in geographic regions where climate variables are spatially decoupled. These regions may represent valuable reservoirs of heritable adaptive phenotypic variation.

Physiological and antioxidant responses of synthetic hexaploid wheat germplasm under drought

BackgroundAs a result of the world population and climate change impact increases (especially in arid environments), there is a critical need for high-yield, drought-tolerant wheat. Synthetic hexaploid wheat derived lines (SHW-DL), were created artificially by crossing different durum wheat cultivars (AABB) with accessions of Aegilops tauschii (DD), a beneficial source of new genes for common bread wheat (Triticum aestivum L). Here, we studied the response of a panel of 91 SHW-DL for drought tolerance based on physiological, antioxidant enzyme activities, and drought tolerance indices.ResultsA wide range of variation and high values of heritability observed for grain yield, physiological and antioxidant traits indicating that the SHW-DL panel constitutes a valuable gene source for drought tolerance improvement of wheat. Despite decreases in grain yield (YLD), leaf area index (LAI), and relative water content (RWC) an increase in the content of malondialdehyde (MDA) was observed. Moreover, drought streass increased the antioxidant enzyme activities of ascorbate peroxidase (APX), catalase (CAT) and peroxidase (POD), and also photosynthetic pigments, proline (Pro), and MDA content. With higher values of grain yield, physiological and biochemical traits such as photosynthetic pigments, and RWC, and lower content of MDA, and peroxidase (H2O2) activity, SHW-DL performed better compared to common wheat lines under water stress conditions.ConclusionsDifferent responses to water stress within the germplasm and between synthetic and common wheat suggest that selection for adaptive and suitable genotypes is possible for drought tolerance in synthetic wheat germplasm. Genotypes 54, 98, 102, 105, 122, 124, 143, 159, 196, and 198 were identified to be directly used in breeding programs or indirectly by crossing them with other wheat germplasm collections.

Natural selection requires no teleology in addition to heritable variation in fitness

According to the standard formulation, natural selection requires variation, differential fitness, and heritability. I argue that this formulation is inadequate because it fails to distinguish natural selection from artificial selection, intelligent design, forward-looking orthogenetic selection, and adaptation via the selection of nonrandom variation. I suggest adding a no teleology condition. The no teleology condition says that the evolutionary process is not guided toward an endpoint represented in the mind of an agent, variation is produced randomly with respect to adaptation, and selection pressures are not forward looking.

Genomics of natural populations: gene conversion events reveal selected genes within the inversions of Drosophila pseudoobscura.

When adaptive phenotypic variation or quantitative trait loci map within an inverted segment of a chromosome, researchers often despair because the suppression of crossing over will prevent the discovery of selective target genes that established the rearrangement. If an inversion polymorphism is old enough, then the accumulation of gene conversion tracts offers the promise that quantitative trait loci or selected loci within inversions can be mapped. The inversion polymorphism of Drosophila pseudoobscura is a model system to show that gene conversion analysis is a useful tool for mapping selected loci within inversions. D. pseudoobscura has over 30 different chromosomal arrangements on the third chromosome (Muller C) in natural populations and their frequencies vary with changes in environmental habitats. Statistical tests of five D. pseudoobscura gene arrangements identified outlier genes within inverted regions that had potentially heritable variation, either fixed amino acid differences or differential expression patterns. We use genome sequences of the inverted third chromosome (Muller C) to infer 98,443 gene conversion tracts for a total coverage of 142 Mb or 7.2× coverage of the 19.7 Mb chromosome. We estimated gene conversion tract coverage in the 2,668 genes on Muller C and tested whether gene conversion coverage was similar among arrangements for outlier vs non-outlier loci. Outlier genes had lower gene conversion tract coverage among arrangements than the non-outlier genes suggesting that selection removes exchanged DNA in the outlier genes. These data support the hypothesis that the third chromosome in D. pseudoobscura captured locally adapted combinations of alleles prior to inversion mutation events.