Genome‐wide association study for body weight in cattle populations from Siberia

Body weight is a complex trait in cattle associated with commonly used commercial breeding measurements related to growth. Although many quantitative trait loci (QTL) for body weight have been identified in cattle so far, searching for genetic determinants in different breeds or environments is promising. Therefore, we carried out a genome‐wide association study (GWAS) in two cattle populations from the Russian Federation (Siberian region) using the GGP HD150K array containing 139 376 single nucleotide polymorphism (SNP) markers. Association tests for 107 550 SNPs left after filtering revealed five statistically significant SNPs on BTA5, considering a false discovery rate of less than 0.05. The chromosomal region containing these five SNPs contains the CCND2 gene, which was previously associated with average daily weight gain and body mass index in US beef cattle populations and in humans respectively. Our study is the first GWAS for body weight in beef cattle populations from the Russian Federation. The results provided here suggest that, despite the existence of breed‐ and species‐specific QTL, the genetic architecture of body weight could be evolutionarily conserved in mammals.     

Identification of candidate genes and mutations in QTL regions for immune responses in chicken

There are two categories of immune responses – innate and adaptive immunity – both having polygenic backgrounds and a significant environmental component. In our study, adaptive immunity was represented by the specific antibody response toward keyhole limpet hemocyanin (KLH); innate immunity was represented by natural antibodies toward lipopolysaccharide (LPS) and lipoteichoic acid (LTA). Defining genetic bases of immune responses leads from defining quantitative trait loci (QTL) toward a single mutation responsible for variation in the phenotypic trait. The goal of the reported study was to define candidate genes and mutations for the immune traits of interest in chicken by performing an association study of SNPs located in candidate genes defined in QTL regions. Candidate genes and SNPs in QTL regions were selected in silico. SNP association was based on a custom SNP panel, GoldenGate genotyping assay (Illumina) and two statistical models: random mixed model and CAR score. The most significant SNP for immune response toward KLH was located in the JMJD6 gene located on GGA18. Four SNPs in candidate genes FOXJ1 (GGA18), EPHB1 (GGA9), PTGER4 (GGAZ) and PRKCB (GGA14) showed association with natural antibodies for LPS. A single SNP in ITGB4 (GGA18) was associated with natural antibodies for LTA. All associated SNPs mentioned above showed additive effects.     

Transcending data gaps: a framework to reduce inferential errors in ecological analyses

The analysis of functional diversity (FD) has gained increasing importance due to its generality and utility in ecology. In particular, patterns in the spatial distribution and temporal change of FD are being used to predict locations and functional groups that are immediately vulnerable to global changes. A major impediment to the accurate measurement of FD is the pervasiveness of missing data in trait datasets. While such prevalent data gaps can engender misleading inferences in FD analyses, we currently lack any practical guide to handle missing data in trait datasets. Here, we identify significant mismatches between true FD and values derived from datasets that contain missing data. We demonstrate that imputing missing data with a phylogeny‐informed approach reduces the risk of misinterpretation of FD patterns, and provides baseline information against which central questions in ecology can be evaluated.     

Genetic mapping shows intraspecific variation and transgressive segregation for caterpillar‐induced aphid resistance in maize

Plants in nature have inducible defences that sometimes lead to targeted resistance against particular herbivores, but susceptibility to others. The metabolic diversity and genetic resources available for maize (Zea mays) make this a suitable system for a mechanistic study of within‐species variation in such plant‐mediated interactions between herbivores. Beet armyworms (Spodoptera exigua) and corn leaf aphids (Rhopalosiphum maidis) are two naturally occurring maize herbivores with different feeding habits. Whereas chewing herbivore‐induced methylation of 2,4‐dihydroxy‐7‐methoxy‐1,4‐benzoxazin‐3‐one glucoside (DIMBOA‐Glc) to form 2‐hydroxy‐4,7‐dimethoxy‐1,4‐benzoxazin‐3‐one glucoside (HDMBOA‐Glc) promotes caterpillar resistance, lower DIMBOA‐Glc levels favour aphid reproduction. Thus, caterpillar‐induced DIMBOA‐Glc methyltransferase activity in maize is predicted to promote aphid growth. To test this hypothesis, the impact of S. exigua feeding on R. maidis progeny production was assessed using seventeen genetically diverse maize inbred lines. Whereas aphid progeny production was increased by prior caterpillar feeding on lines B73, Ki11, Ki3 and Tx303, it decreased on lines Ky21, CML103, Mo18W and W22. Genetic mapping of this trait in a population of B73 × Ky21 recombinant inbred lines identified significant quantitative trait loci on maize chromosomes 1, 7 and 10. There is a transgressive segregation for aphid resistance, with the Ky21 alleles on chromosomes 1 and 7 and the B73 allele on chromosome 10 increasing aphid progeny production. The chromosome 1 QTL coincides with a cluster of three maize genes encoding benzoxazinoid O‐methyltransferases that convert DIMBOA‐Glc to HDMBOA‐Glc. Gene expression studies and benzoxazinoid measurements indicate that S. exigua ‐induced responses in this pathway differentially affect R. maidis resistance in B73 and Ky21.     

Drought stress limits the geographic ranges of two tree species via different physiological mechanisms

Range shifts are among the most ubiquitous ecological responses to anthropogenic climate change and have large consequences for ecosystems. Unfortunately, the ecophysiological forces that constrain range boundaries are poorly understood, making it difficult to mechanistically project range shifts. To explore the physiological mechanisms by which drought stress controls dry range boundaries in trees, we quantified elevational variation in drought tolerance and in drought avoidance‐related functional traits of a widespread gymnosperm (ponderosa pine – Pinus ponderosa) and angiosperm (trembling aspen – Populus tremuloides) tree species in the southwestern USA. Specifically, we quantified tree‐to‐tree variation in growth, water stress (predawn and midday xylem tension), drought avoidance traits (branch conductivity, leaf/needle size, tree height, leaf area‐to‐sapwood area ratio), and drought tolerance traits (xylem resistance to embolism, hydraulic safety margin, wood density) at the range margins and range center of each species. Although water stress increased and growth declined strongly at lower range margins of both species, ponderosa pine and aspen showed contrasting patterns of clinal trait variation. Trembling aspen increased its drought tolerance at its dry range edge by growing stronger but more carbon dense branch and leaf tissues, implying an increased cost of growth at its range boundary. By contrast, ponderosa pine showed little elevational variation in drought‐related traits but avoided drought stress at low elevations by limiting transpiration through stomatal closure, such that its dry range boundary is associated with limited carbon assimilation even in average climatic conditions. Thus, the same climatic factor (drought) may drive range boundaries through different physiological mechanisms – a result that has important implications for process‐based modeling approaches to tree biogeography. Further, we show that comparing intraspecific patterns of trait variation across ranges, something rarely done in a range‐limit context, helps elucidate a mechanistic understanding of range constraints.     

Genomic analyses of a “living fossil”: The endangered dove‐tree

Davidia involucrata Baill, also known as the dove‐tree, is a living fossil and an endangered species currently restricted to the mountains of southwestern and central China. It has a beautiful and innovative trait of high horticultural value: two white bracts covering the flower caputila. Here, we report on the chromosome‐scale genome of this species using single‐molecule real‐time long reads and chromosome conformation capture (Hi‐C) techniques. This species has a larger genome size of 1,169 Mb and contains relatively more genes (42,554) than the closely related species Camptotheca acuminata (397 Mb and 31,825 genes). Both species shared one recent whole genome duplication before their divergence. The expansion of the repetitive elements after their divergence contributed greatly to the increase in the genome size of the dove‐tree. Photosynthesis‐related genes were almost absent or showed reduced expression in the bracts of the dove‐tree, while defence‐ and chemical‐related genes increased greatly, highlighting the important roles of the bracts in protecting flowers and attracting pollinators. The effective population size of the dove‐tree continuously decreased during the climate changes of the Quaternary. Such climate sensitivity should be fully considered in conservation efforts for this relict endangered species in the context of continuous climate warming in the future.     

On the use of the transmission disequilibrium test to detect pseudo‐autosomal variants affecting traits with sex‐limited expression

We herein describe the realization of a genome‐wide association study for scrotal hernia and cryptorchidism in Norwegian and Belgian commercial pig populations. We have used the transmission disequilibrium test to avoid spurious associations due to population stratification. By doing so, we obtained genome‐wide significant signals for both diseases with SNPs located in the pseudo‐autosomal region in the vicinity of the pseudo‐autosomal boundary. By further analyzing these signals, we demonstrate that the observed transmission disequilibria are artifactual. We determine that transmission bias at pseudo‐autosomal markers will occur (i) when analyzing traits with sex‐limited expression and (ii) when the allelic frequencies at the marker locus differ between X and Y chromosomes. We show that the bias is due to the fact that (i) sires will preferentially transmit the allele enriched on the Y (respectively X) chromosome to affected sons (respectively daughters) and (ii) dams will appear to preferentially transmit the allele enriched on the Y (respectively X) to affected sons (respectively daughters), as offspring inheriting the other allele are more likely to be non‐informative. We define the conditions to mitigate these issues, namely by (i) extracting information from maternal meiosis only and (ii) ignoring trios for which sire and dam have the same heterozygous genotype. We show that by applying these rules to scrotal hernia and cryptorchidism, the pseudo‐autosomal signals disappear, confirming their spurious nature.     

Survival of a specialist natural enemy experiencing resource competition with an omnivorous predator when sharing the invasive prey Tuta absoluta

Can specialist natural enemies persist in ecosystems when competing with omnivorous natural enemies for their shared prey? The consequences of omnivory have been studied theoretically, but empirical studies are still lacking. Omnivory is nevertheless common in nature and omnivorous predators coexist with specialists in many ecosystems, even when they are intraguild predators. This type of association is also common in agroecosystems in which biological control strategies are used. Our study provides an example of the outcome of such an association in the context of biological control of the invasive pest Tuta absoluta (Lepidoptera) in a tomato agroecosystem. The two natural enemies involved, that is, a specialist (Stenomesius japonicus (Hymenoptera) parasitoid) and an omnivore (Macrolophus pygmaeus (Hemiptera) predator), were able to coexist for 3 months in our experimental cages in the absence of metacommunity mechanisms (i.e., emigration and recolonization), contrary to theoretical expectations. However, they negatively affected each other's population dynamics. We found that spatial resource segregation was not a mechanism that promoted their coexistence. Regarding pest control, the specialist and omnivorous natural enemies were found to exhibit complementary functional traits, leading to the best control when together. Mechanisms that may have promoted the coexistence of the two species as well as consequences with regard to the inoculative biological control program are discussed.     

Artificial selection on larval growth curves in Tribolium: correlated responses and constraints

Body size is often constrained from evolving. Although artificial selection on body size in insects frequently results in a sizable response, these responses usually bear fitness costs. Further, these experiments tend to select only on size at one landmark age, rather than selecting for patterns of growth over the whole larval life stage. To address whether constraints may be caused by larval growth patterns rather than final size, we implemented a function‐valued (FV) trait method of selection, in which entire larval growth curves from Tribolium were artificially selected. The selection gradient function used was previously predicted to give the maximal response and was implemented using a novel selection index in the FV framework. Results indicated a significant response after one generation of selection, but no response in subsequent generations. Correlated responses included increased mortality, increased critical weight, and decreased development time (DT). The lack of response in size and development time after the first generation was likely caused by increased mortality suffered in selected lines; we demonstrated that the selection criterion caused both increased body size and increased mortality. We conclude that artificial selection on continuous traits using FV methods is very efficient and that the constraint of body size evolution is likely caused by a suite of trade‐offs with other traits.     

Clustering of loci controlling species differences in male chemical bouquets of sympatric Heliconius butterflies

The degree to which loci promoting reproductive isolation cluster in the genome—that is, the genetic architecture of reproductive isolation—can influence the tempo and mode of speciation. Tight linkage between these loci can facilitate speciation in the face of gene flow. Pheromones play a role in reproductive isolation in many Lepidoptera species, and the role of endogenously produced compounds as secondary metabolites decreases the likelihood of pleiotropy associated with many barrier loci. Heliconius butterflies use male sex pheromones to both court females (aphrodisiac wing pheromones) and ward off male courtship (male‐transferred antiaphrodisiac genital pheromones), and it is likely that these compounds play a role in reproductive isolation between Heliconius species. Using a set of backcross hybrids between H. melpomene and H. cydno, we investigated the genetic architecture of putative male pheromone compound production. We found a set of 40 significant quantitative trait loci (QTL) representing 33 potential pheromone compounds. QTL clustered significantly on two chromosomes, chromosome 8 for genital compounds and chromosome 20 for wing compounds, and chromosome 20 was enriched for potential pheromone biosynthesis genes. There was minimal overlap between pheromone QTL and known QTL for mate choice and color pattern. Nonetheless, we did detect linkage between a QTL for wing androconial area and optix, a color pattern locus known to play a role in reproductive isolation in these species. This tight clustering of putative pheromone loci might contribute to coincident reproductive isolating barriers, facilitating speciation despite ongoing gene flow.     

Characterizing drought stress and trait influence on maize yield under current and future conditions

Global climate change is predicted to increase temperatures, alter geographical patterns of rainfall and increase the frequency of extreme climatic events. Such changes are likely to alter the timing and magnitude of drought stresses experienced by crops. This study used new developments in the classification of crop water stress to first characterize the typology and frequency of drought‐stress patterns experienced by European maize crops and their associated distributions of grain yield, and second determine the influence of the breeding traits anthesis‐silking synchrony, maturity and kernel number on yield in different drought‐stress scenarios, under current and future climates. Under historical conditions, a low‐stress scenario occurred most frequently (ca. 40%), and three other stress types exposing crops to late‐season stresses each occurred in ca. 20% of cases. A key revelation shown was that the four patterns will also be the most dominant stress patterns under 2050 conditions. Future frequencies of low drought stress were reduced by ca. 15%, and those of severe water deficit during grain filling increased from 18% to 25%. Despite this, effects of elevated CO₂ on crop growth moderated detrimental effects of climate change on yield. Increasing anthesis‐silking synchrony had the greatest effect on yield in low drought‐stress seasonal patterns, whereas earlier maturity had the greatest effect in crops exposed to severe early‐terminal drought stress. Segregating drought‐stress patterns into key groups allowed greater insight into the effects of trait perturbation on crop yield under different weather conditions. We demonstrate that for crops exposed to the same drought‐stress pattern, trait perturbation under current climates will have a similar impact on yield as that expected in future, even though the frequencies of severe drought stress will increase in future. These results have important ramifications for breeding of maize and have implications for studies examining genetic and physiological crop responses to environmental stresses.     

Little association of biological trait values with environmental variables in invasive alien round goby (Neogobius melanostomus)

The relative importance of species‐specific biological trait characteristics and environmental factors in invasions of nonindigenous species remains controversial because both have mostly been studied independently. Thus, the main objective of this study was to examine the correlation of biological traits with environmental variation in the globally invasive round goby Neogobius melanostomus from the upper Danube River. Based on a sample of 653 specimens along a continuous 200 km river pathway, links between nine environmental factors (substrate‐type, six water measurements, and the communities of fishes and macroinvertebrates) and seven biological traits (nutritional and energetic status, trade‐offs of parasite resistance and resource allocation, and three growth proxies) were analyzed. Biological trait values of N. melanostomus hardly correlated with the environment, could not explain invasion progress and imply a general low overall importance for invasion success. Instead, alternative individual life‐history trajectories appear to determine invasion success. This is in line with up to 15% of all specimens having outlying biological trait values of potential adaptive value, suggesting a considerable importance of adaptive trait variation among single individuals for the whole invasion progress. This “individual trait utility hypothesis” gives an alternative explanation for success of invasive species by single individuals carrying particular traits, and it should be specifically targeted and analyzed at currently invaded sites.     

Quantitative trait loci for growth and body size in the nine‐spined stickleback Pungitius pungitius L.

Body size is an ecologically important trait shown to be genetically variable both within and among different animal populations as revealed by quantitative genetic studies. However, few studies have looked into underlying genetic architecture of body size variability in the wild using genetic mapping methods. With the aid of quantitative trait loci (QTL) analyses based on 226 microsatellite markers, we mapped body size and growth rate traits in the nine‐spined stickleback (Pungitius pungitius) using an F₂‐intercross (n = 283 offspring) between size‐divergent populations. In total, 17 QTL locations were detected. The proportion of phenotypic variation explained by individual body size‐related QTL ranged from 3% to 12% and those related to growth parameters and increments from 3% to 10%. Several of the detected QTL affected either early or late growth. These results provide a solid starting point for more in depth investigations of structure and function of genomic regions involved in determination of body size in this popular model of ecological and evolutionary research.     

Adenylate cyclase 5 is required for melanophore and male pattern development in the guppy (Poecilia reticulata)

Guppies (Poecilia reticulata) are colorful fish that have attracted the attention of pigmentation researchers for almost a century. Here, we report that the blond phenotype of the guppy is caused by a spontaneous mutation in the guppy ortholog of adenylate cyclase 5 (adcy5). Using double digest restriction site‐associated DNA sequencing (ddRADseq) and quantitative trait locus (QTL) mapping, we linked the blond phenotype to a candidate region of 118 kb, in which we subsequently identified a 2‐bp deletion in adcy5 that alters splicing and leads to a premature stop codon. We show that adcy5, which affects life span and melanoma growth in mouse, is required for melanophore development and formation of male orange pigmentation traits in the guppy. We find that some components of the male orange pattern are particularly sensitive to loss of Adcy5 function. Our work thus reveals a function for Adcy5 in patterning of fish color ornaments.     

Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds

Successful urban colonization by formerly rural species represents an ideal situation in which to study adaptation to novel environments. We address this issue using candidate genes for behavioural traits that are expected to play a role in such colonization events. We identified and genotyped 16 polymorphisms in candidate genes for circadian rhythms, harm avoidance and migratory and exploratory behaviour in 12 paired urban and rural populations of the blackbird Turdus merula across the Western Palaearctic. An exonic microsatellite in the SERT gene, a candidate gene for harm avoidance behaviour, exhibited a highly significant association with habitat type in an analysis conducted across all populations. Genetic divergence at this locus was consistent in 10 of the 12 population pairs; this contrasts with previously reported stochastic genetic divergence between these populations at random markers. Our results indicate that behavioural traits related to harm avoidance and associated with the SERT polymorphism experience selection pressures during most blackbird urbanization events. These events thus appear to be influenced by homogeneous adaptive processes in addition to previously reported demographic founder events.