Molecular diversity and landscape genomics of the crop wild relative Triticum urartu across the Fertile Crescent

Modern plant breeding can benefit from the allelic variation that exists in natural populations of crop wild relatives that evolved under natural selection in varying pedoclimatic conditions. In this study, next‐generation sequencing was used to generate 1.3 million genome‐wide single nucleotide polymorphisms (SNPs) on ex situ collections of Triticum urartu L., the wild donor of the A^u subgenome of modern wheat. A set of 75 511 high‐quality SNPs were retained to describe 298 T. urartu accessions collected throughout the Fertile Crescent. Triticum urartu showed a complex pattern of genetic diversity, with two main genetic groups distributed sequentially from west to east. The incorporation of geographical information on sampling points showed that genetic diversity was correlated to the geographical distance (R² = 0.19) separating samples from Jordan and Lebanon, from Syria and southern Turkey, and from eastern Turkey, Iran and Iraq. The wild emmer genome was used to derive the physical positions of SNPs on the seven chromosomes of the A^u subgenome, allowing us to describe a relatively slow decay of linkage disequilibrium in the collection. Outlier loci were described on the basis of the geographic distribution of the T. urartu accessions, identifying a hotspot of directional selection on chromosome 4A. Bioclimatic variation was derived from grid data and related to allelic variation using a genome‐wide association approach, identifying several marker–environment associations (MEAs). Fifty‐seven MEAs were associated with altitude and temperature measures while 358 were associated with rainfall measures. The most significant MEAs and outlier loci were used to identify genomic loci with adaptive potential (some already reported in wheat), including dormancy and frost resistance loci. We advocate the application of genomics and landscape genomics on ex situ collections of crop wild relatives to efficiently identify promising alleles and genetic materials for incorporation into modern crop breeding.     

Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change

Climate change is expected to alter the dynamics of host–parasite systems globally. One key element in developing predictive models for these impacts is the life cycle of the parasite. It is, for example, commonly assumed that parasites with an indirect life cycle would be more sensitive to changing environmental conditions than parasites with a direct life cycle due to the greater chance that at least one of their obligate host species will go extinct. Here, we challenge this notion by contrasting parasitic nematodes with a direct life cycle against those with an indirect life cycle. Specifically, we suggest that behavioral thermoregulation by the intermediate host may buffer the larvae of indirectly transmitted parasites against temperature extremes, and hence climate warming. We term this the ‘shelter effect’. Formalizing each life cycle in a comprehensive model reveals a fitness advantage for the direct life cycle over the indirect life cycle at low temperatures, but the shelter effect reverses this advantage at high temperatures. When examined for seasonal environments, the models suggest that climate warming may in some regions create a temporal niche in mid‐summer that excludes parasites with a direct life cycle, but allows parasites with an indirect life cycle to persist. These patterns are amplified if parasite larvae are able to manipulate their intermediate host to increase ingestion probability by definite hosts. Furthermore, our results suggest that exploiting the benefits of host sheltering may have aided the evolution of indirect life cycles. Our modeling framework utilizes the Metabolic Theory of Ecology to synthesize the complexities of host behavioral thermoregulation and its impacts on various temperature‐dependent parasite life history components in a single measure of fitness, R₀. It allows quantitative predictions of climate change impacts, and is easily generalized to many host–parasite systems.     

Investigation of Mannheimia haemolytica bacteriophages relative to host diversity

Aims

This study aimed to characterize the impact of lytic and temperate bacteriophages on the genetic and phenotypic diversity of Mannheimia haemolytica from feedlot cattle.

Methods and Results

Strictly lytic phages were not detected from bovine nasopharyngeal (n = 689) or water trough (n = 30) samples, but Myoviridae‐ or Siphoviridae‐like phages were induced from 54 of 72 M. haemolytica strains by mitomycin C, occasionally from the same strain. Phages with similar restriction fragment length polymorphism profiles (RFLP ≥70% relatedness) shared common host serotypes 1 or 2 (P < 0·000 1). Likewise, phages with similar RFLP tended to occur in genetically related host bacteria (70–79% similarity). Host range assays showed that seven phages from host serotypes 1, 2 and 6 lysed representative strains of serotypes 1, 2 or 8. The genome of vB_MhM_1152AP from serotype 6 was found to be collinear with P2‐like phage φMhaA1‐PHL101.

Conclusions

Prophages are a significant component of the genome of M. haemolytica and contribute significantly to host diversity. Further characterization of the role of prophage in virulence and persistence of M. haemolytica in cattle could provide insight into approaches to control this potential respiratory pathogen.

Significance and Impact of the Study

This study demonstrated that prophages are widespread within the genome of M. haemolytica isolates and emphasized the challenge of isolating lytic phage as a therapeutic against this pathogen.     

Evolution of dentition in salamanders: relative roles of phylogeny and diet

Despite being widely regarded as generalist predators, amphibians exhibit a diversity of tooth shapes and dentition patterns, which may indicate the influence of dietary specialization on the evolution of tooth morphology. Very few studies have analysed the relationship between tooth morphology and diet (i.e., prey items) in amphibians, and those existing studies are highly speculative. We investigated the evolution of salamander teeth and the relationship between tooth morphology and diet in a phylogenetically independent fashion. We used a phylogeny of 23 species of salamander representing three families (Ambystomatidae, Plethodontidae, and Salamandridae) to, first, analyse the divergence of tooth morphology and its relationship to phylogeny and, second, to analyse the relationship between tooth morphology and diet diversity. We used electron scanning microscopy and a statistical comparative approach using Spatial Evolutionary and Ecological Analysis (SEEVA) and phylogenetic generalized least‐squares regression in R. Our results indicated significant divergence in tooth morphology at major phylogenetic splits. Moreover, there was a significant, phylogenetically independent relationship between tooth morphology and diet diversity. The relationship between diet and tooth morphology indicates not only a reflection of phylogenetic history, but also a degree of dietary specialization, indicating that evolution in tooth morphology has had an adaptive aspect in relation to salamander diet.     

Large‐scale adaptive divergence in Boechera fecunda,an endangered wild relative of Arabidopsis

Many biological species are threatened with extinction because of a number of factors such as climate change and habitat loss, and their preservation depends on an accurate understanding of the extent of their genetic variability within and among populations. In this study, we assessed the genetic divergence of five quantitative traits in 10 populations of an endangered cruciferous species, Boechera fecunda, found in only several populations in each of two geographic regions (WEST and EAST) in southwestern Montana. We analyzed variation in quantitative traits, neutral molecular markers, and environmental factors and provided evidence that despite the restricted geographical distribution of this species, it exhibits a high level of genetic variation and regional adaptation. Conservation efforts therefore should be directed to the preservation of populations in each of these two regions without attempting transplantation between regions. Heritabilities and genetic coefficients of variation estimated from nested ANOVAs were generally high for leaf and rosette traits, although lower (and not significantly different from 0) for water‐use efficiency. Measures of quantitative genetic differentiation, Q_ST, were calculated for each trait from each pair of populations. For three of the five traits, these values were significantly higher between regions compared with those within regions (after adjustment for neutral genetic variation, F_ST). This suggested that natural selection has played an important role in producing regional divergence in this species. Our analysis also revealed that the B. fecunda populations appear to be locally adapted due, at least in part, to differences in environmental conditions in the EAST and WEST regions.     

Population structure of two rabies hosts relative to the known distribution of rabies virus variants in Alaska

For pathogens that infect multiple species, the distinction between reservoir hosts and spillover hosts is often difficult. In Alaska, three variants of the arctic rabies virus exist with distinct spatial distributions. We tested the hypothesis that rabies virus variant distribution corresponds to the population structure of the primary rabies hosts in Alaska, arctic foxes (Vulpes lagopus) and red foxes (Vulpes vulpes) to possibly distinguish reservoir and spillover hosts. We used mitochondrial DNA (mtDNA) sequence and nine microsatellites to assess population structure in those two species. mtDNA structure did not correspond to rabies virus variant structure in either species. Microsatellite analyses gave varying results. Bayesian clustering found two groups of arctic foxes in the coastal tundra region, but for red foxes it identified tundra and boreal types. Spatial Bayesian clustering and spatial principal components analysis identified 3 and 4 groups of arctic foxes, respectively, closely matching the distribution of rabies virus variants in the state. Red foxes, conversely, showed eight clusters comprising two regions (boreal and tundra) with much admixture. These results run contrary to previous beliefs that arctic fox show no fine‐scale spatial population structure. While we cannot rule out that the red fox is part of the maintenance host community for rabies in Alaska, the distribution of virus variants appears to be driven primarily by the arctic fox. Therefore, we show that host population genetics can be utilized to distinguish between maintenance and spillover hosts when used in conjunction with other approaches.     

Oviposition preferences in Grapholita molesta: the relative importance of visual and olfactory cues

The oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae), is a major pest of fruit trees worldwide. Females oviposit on the young leaves of peach [Prunus persica (L.) Batsch (Rosaceae)] shoots at twilight, when light intensity changes markedly. Previous researches have shown that the oviposition response of this moth is guided particularly by visual and olfactory cues from host plants. However, the relative importance of visual and olfactory cues in their oviposition preference is largely unknown. As a crepuscular moth, how do choices change as light intensity drops rapidly from day to night? In the present study, through two‐choice behavioural experiments, the oviposition responses of G. molesta to visual and olfactory cues (alone or in combination) from peach shoots were tested at four light intensities ranging from daylight to starlight. Grapholita molesta showed similar oviposition responses to plant cues under 1 000, 100, 1 and 0.01 mW m^?2 illumination. Olfactory cues from peach shoots attracted significantly more oviposition than the negative control, whereas visual cues alone did not. Furthermore, olfactory cues were more attractive than visual cues, and no significant interaction was observed between the responses to the two cues. Our findings indicate that G. molesta females mainly rely on olfactory cues to recognize oviposition sites, regardless of differences in light intensity. These results do not provide evidence for attraction to visual cues, but the possibility that the brightness of leaves might be used to guide oviposition is discussed.     

Elevational diversity gradients of Tibetan loaches: The relative roles of ecological and evolutionary processes

It is widely believed that species richness patterns (SRPs) are shaped by both ecological and evolutionary processes. However, the relative roles of these processes remain unclear, especially for aquatic organisms. In this study, we integrated ecological and evolutionary measures to tease apart the relative influences of these factors on the SRP of Tibetan loaches along an extensive elevational gradient. We found that the Tibetan loaches displayed a richness pattern that peaked at midelevations. The mean annual temperature (MAT), mid‐domain effect (MDE), and summed age of colonization (SAC, complex of colonization age and colonization frequency) were the main drivers, accounting for 85%, 51%, and 88% of the variations in the SRP, respectively. The three predictors had very high combined effects (MAT‐MDE‐SAC, MAT‐SAC, and MDE‐SAC were 44%, 38%, and 6%, respectively). Our analyses suggested that energy input, time‐for‐speciation, and species dispersal may directly guide the SRP or mediate it by geometric constraints. Conclusively, the SRP of the Tibetan loaches with elevation is the outcome of interactions between biogeographical processes and regional ecological conditions.     

Dietary specialization in mutualistic acacia‐ants affects relative abundance but not identity of host‐associated bacteria

Acacia‐ant mutualists in the genus Pseudomyrmex nest obligately in acacia plants and, as we show through stable isotope analysis, feed at a remarkably low trophic level. Insects with diets such as these sometimes depend on bacterial symbionts for nutritional enrichment. We, therefore, examine the bacterial communities associated with acacia‐ants in order to determine whether they host bacterial partners likely to contribute to their nutrition. Despite large differences in trophic position, acacia‐ants and related species with generalized diets do not host distinct bacterial taxa. However, we find that a small number of previously undescribed bacterial taxa do differ in relative abundance between acacia‐ants and generalists, including several Acetobacteraceae and Nocardiaceae lineages related to common insect associates. Comparisons with an herbivorous generalist, a parasite that feeds on acacias and a mutualistic species with a generalized diet show that trophic level is likely responsible for these small differences in bacterial community structure. While we did not experimentally test for a nutritional benefit to hosts of these bacterial lineages, metagenomic analysis reveals a Bartonella relative with an intact nitrogen‐recycling pathway widespread across Pseudomyrmex mutualists and generalists. This taxon may be contributing to nitrogen enrichment of its ant hosts through urease activity and, concordant with an obligately host‐associated lifestyle, appears to be experiencing genomewide relaxed selection. The lack of distinctiveness in bacterial communities across trophic level in this group of ants shows a remarkable ability to adjust to varied diets, possibly with assistance from these diverse ant‐specific bacterial lineages.     

The relative availability of inorganic carbon and inorganic nitrogen influences the response of the dinoflagellate Protoceratium reticulatum to elevated CO2

This work originates from three facts: (i) changes in CO₂ availability influence metabolic processes in algal cells; (ii) Spatial and temporal variations of nitrogen availability cause repercussions on phytoplankton physiology; (iii) Growth and cell composition are dependent on the stoichiometry of nutritional resources. In this study, we assess whether the impact of rising pCO₂ is influenced by N availability, through the impact that it would have on the C/N stoichiometry, in conditions of N sufficiency. Our experiments used the dinoflagellate Protoceratium reticulatum, which we cultured under three CO₂ regimes (400, 1,000, and 5,000 ppmv, pH of 8.1) and either variable (the NO₃^? concentration was always 2.5 mmol · L^?1) or constant (NO₃^? concentration varied to maintain the same C_i/NO₃^? ratio at all pCO₂) C_i/NO₃^? ratio. Regardless of N availability, cells had higher specific growth rates, but lower cell dry weight and C and N quotas, at elevated CO₂. The carbohydrate pool size and the C/N was unaltered in all treatments. The lipid content only decreased at high pCO₂ at constant C_i/NO₃^? ratio. In the variable C_i/NO₃^? conditions, the relative abundance of Rubisco (and other proteins) also changed; this did not occur at constant C_i/NO₃^?. Thus, the biomass quality of P. reticulatum for grazers was affected by the C_i/NO₃^? ratio in the environment and not only by the pCO₂, both with respect to the size of the main organic pools and the composition of the expressed proteome.     

Differences in perceived predation risk associated with variation in relative size of extra‐pair and within‐pair offspring

Extra‐pair paternity (EPP) is a widespread phenomenon in birds. Researchers have long hypothesized that EPP must confer a fitness advantage to extra‐pair offspring (EPO), but empirical support for this hypothesis is definitively mixed. This could be because genetic benefits of EPP only exist in a subset of environmental contexts to which a population is exposed. From 2013 to 2015, we manipulated perceived predator density in a population of tree swallows (Tachycineta bicolor) breeding in New York to see whether fitness outcomes of extra‐pair and within‐pair offspring (WPO) varied with predation risk. In nests that had been exposed to predators, EPO were larger, longer‐winged and heavier than WPO. In nonpredator nests, WPO tended to be larger, longer‐winged and heavier than EPO, though the effect was nonsignificant. We found no differences in age, morphology or stress physiology between extra‐pair and within‐pair sires from the same nest, suggesting that additive genetic benefits cannot fully explain the differences in nestling size that we observed. The lack of an effect of predator exposure on survival or glucocorticoid stress physiology of EPO and WPO further suggests that observed size differences do not reflect more general variation in intrinsic genetic quality. Instead, we suggest that size differences may have arisen through differential investment into EPO and WPO by females, perhaps because EPO and WPO represent different reproductive strategies, with each type of nestling conferring a fitness advantage in specific ecological contexts.     

Filamentous cyanobacteria alter the relative fitness in a Daphnia hybrid species complex

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Belowground interactions shift the relative importance of direct and indirect genetic effects

Intraspecific genetic variation can affect decomposition, nutrient cycling, and interactions between plants and their associated belowground communities. However, the effects of genetic variation on ecosystems can also be indirect, meaning that genes in a focal plant may affect ecosystems by altering the phenotype of interacting (i.e., neighboring) individuals. We manipulated genotype identity, species identity, and the possibility of belowground interactions between neighboring Solidago plants. We hypothesized that, because our plants were nitrogen (N) limited, the most important interactions between focal and neighbor plants would occur belowground. More specifically, we hypothesized that the genotypic identity of a plant's neighbor would have a larger effect on belowground biomass than on aboveground biomass, but only when neighboring plants were allowed to interact belowground. We detected species‐ and genotype‐level variation for aboveground biomass and ramet production. We also found that belowground biomass and ramet production depended on the interaction of neighbor genotype identity and the presence or absence of belowground interactions. Additionally, we found that interspecific indirect genetic effects (IIGEs; changes in focal plant traits due to the genotype identity of a heterospecific neighbor) had a greater effect size on belowground biomass than did focal genotype; however, this effect only held in pots that allowed belowground interactions. These results expand the types of natural processes that can be attributed to genotypes by showing that, under certain conditions, a plant's phenotype can be strongly determined by the expression of genes in its neighbor. By showing that IIGEs are dependent upon plants being able to interact belowground, our results also provide a first step for thinking about how genotype‐based, belowground interactions influence the evolutionary outcomes of plant‐neighbor interactions.     

Tetracycline‐exposed Drosophila melanogaster males produce fewer offspring but a relative excess of sons

A large diversity of species possesses endosymbionts; these endosymbionts can exhibit mutualistic, parasitic, and commensal relationships with their hosts. Previous work has consistently revealed that depleting endosymbiont titer with antibiotic treatment can significantly alter host fitness and function, particularly with respect to reproductive phenotypes. Although these findings are often interpreted as resulting from the breakdown of highly coevolved symbioses, it is possible that antibiotic treatment itself rather than endosymbiont removal contributes to the observed perturbations in reproductive phenotypes. Here, we investigate the effect of tetracycline treatment on sex ratio and male reproductive fitness using Drosophila melanogaster as a model system. Our results indicate that tetracycline‐treated males produce a relative excess of sons. We also find that tetracycline treatment reduces the number of progeny produced by treated males but not treated females. These findings are independent of the effects of tetracycline on Wolbachia titer and implicate the antibiotic itself as mediating these changes. It is yet unclear whether the sex ratio shift and reduction in male reproductive fitness are direct or indirect consequences of tetracycline exposure, and more work is needed to determine the molecular mechanisms by which these disturbances in reproductive phenotypes arise. Our data highlight the importance of considering the potentially confounding effects of antibiotic treatment when investigating the effects of endosymbiont depletion on host phenotypes.     

Quantifying the relative predation pressure on bumblebee nests by the European badger (Meles meles) using artificial nests

Bumblebee populations are declining. Factors that impact the size and success of colonies act by either limiting resource availability (bottom‐up regulation) or causing mortality, for example, pesticides, disease, and possibly predation (top‐down regulation). The impact of predation has not been quantified, and so, the current study used novel artificial nests as a proxy for wild bumblebee nests to quantify the relative predation pressure from badgers in two habitats: woodland and grassland, and at two nesting depths: surface and underground. Badgers occur across most parts of the UK and are known to predate on bumblebee nests. We found that significantly more artificial nests (pots containing bumblebee nest material) were dug up compared with control pots (pots without bumblebee nest material). This shows that artificial nests have the potential to be used as a method to study the predation of bumblebee nests by badgers. In a location of high badger density, predation pressure was greater in woodland than grassland, whereas no difference was observed in relation to nest depth. Woodland and grassland are shared habitats between bumblebees and badgers, and we suggest that higher predation may relate to activity and foraging behavior of badgers in woodland compared with grassland. We discuss how badger predation in different habitats could impact different bumblebee species according to their nesting behaviors. Understanding the relative impact of badger predation on bumblebee colonies provides key information on how such top‐down regulation affects bumblebee populations.     

Field evaluation of the relative attractiveness of enriched ginger root oil (EGO)lure and trimedlure for African Ceratitis species (Diptera: Tephritidae)

The males of some fruit flies (Diptera: Tephritidae) are known to be attracted to specific parapheromones. The trapping results between trimedlure (TML) and enriched ginger root oil (EGOlure) were compared at two experimental sites in Morogoro (Central Tanzania) for a period of 12 weeks co‐inciding with the main citrus season. Both attractants captured a comparable diversity of fruit flies, except that EGOlure also attracted fruit flies, such as Ceratitis cosyra, not normally found in TML‐baited traps. Both EGOlure and TML attracted mainly or exclusively male fruit flies, but the catches with EGOlure were equal or superior to those with TML. It is concluded that EGOlure should be considered as a suitable alternative for TML in detection, monitoring and control programs for African fruit flies of the genus Ceratitis. It has the added advantage that it combines the attractiveness with regard to species spectrum of both TML and terpinyl acetate.