Temperature and population density: interactional effects of environmental factors on phenotypic plasticity,immune defenses,and disease resistance in an insect pest

Temperature and crowding are key environmental factors mediating the transmission and epizooty of infectious disease in ectotherm animals. The host physiology may be altered in a temperature‐dependent manner and thus affects the pathogen development and course of diseases within an individual and host population, or the transmission rates (or infectivity) of pathogens shift linearly with the host population density. To our understanding, the knowledge of interactive and synergistic effects of temperature and population density on the host–pathogen system is limited. Here, we tested the interactional effects of these environmental factors on phenotypic plasticity, immune defenses, and disease resistance in the velvetbean caterpillar Anticarsia gemmatalis. Upon egg hatching, caterpillars were reared in thermostat‐controlled chambers in a 2 × 4 factorial design: density (1 or 8 caterpillars/pot) and temperature (20, 24, 28, or 32°C). Of the immune defenses assessed, encapsulation response was directly affected by none of the environmental factors; capsule melanization increased with temperature in both lone‐ and group‐reared caterpillars, although the lone‐reared ones presented the most evident response, and hemocyte numbers decreased with temperature regardless of the population density. Temperature, but not population density, affected considerably the time from inoculation to death of velvetbean caterpillar. Thus, velvetbean caterpillars succumbed to Anticarsia gemmatalis multiple nucleopolyhedrovirus (AgMNPV) more quickly at higher temperatures than at lower temperatures. As hypothesized, temperature likely affected caterpillars' movement rates, and thus the contact between conspecifics, which in turn affected the phenotypic expression of group‐reared caterpillars. Our results suggest that environmental factors, mainly temperature, strongly affect both the course of disease in velvetbean caterpillar population and its defenses against pathogens. As a soybean pest, velvetbean caterpillar may increase its damage on soybean fields under a scenario of global warming as caterpillars may reach the developmental resistance faster, and thus decrease their susceptibility to biological control by AgMNPV.     

Relationship between maternal transfer of immunity and mother fecundity in an insect

Trans-generational immune priming (TGIP) corresponds to the plastic adjustment of offspring immunity as a result of maternal immune experience. TGIP is expected to improve mother's fitness by improving offspring individual performance in an environment where parasitism becomes more prevalent. However, it was recently demonstrated that maternal transfer of immunity to the offspring is costly for immune-challenged female insects. Thus, these females might not provide immune protection to all their offspring because of the inherent cost of other fitness-related traits. Females are therefore expected to adjust their investment to individual offspring immune protection in ways that maximize their fitness. In this study, we investigated how bacterially immune-challenged females of the mealworm beetle, Tenebrio molitor, provision their eggs with immune protection according to egg production. We found that immune-challenged females provide a variable number of their eggs with internal antibacterial activity along egg-laying bouts. Furthermore, within the first immune-protected egg-laying bout (2-4 days after the maternal immune challenge), the number of eggs protected was strongly dependent on the number of eggs produced. Immune-challenged females might therefore adjust their investment into TGIP and fecundity according of their individual perception of the risk of dying from the infection and the expected parasitic conditions for the offspring.     

Thematic review series: the immune system and atherogenesis. Recent insights into the biology of macrophage scavenger receptors

Scavenger receptors were originally defined by their ability to bind and internalize modified lipoproteins. Macrophages express at least six structurally different cell surface receptors for modified forms of LDL that contribute to foam cell formation in atherosclerosis. In addition to their role in the pathology of atherosclerosis, macrophage scavenger receptors, especially SR-A, play critical roles in innate immunity, apoptotic cell clearance, and tissue homeostasis. In this review, we highlight recent advances in understanding the biology of macrophage scavenger receptors as pattern recognition receptors for both infectious nonself (pathogens) and modified self (apoptotic cells and modified LDL). We critically evaluate the potential of scavenger receptors and their ligands as targets for therapeutic intervention in human disease.     

Thematic review series: the immune system and atherogenesis. Immune function in atherogenesis

In this overview to a new thematic series on the immune system and atherogenesis, I provide a very brief summary of current conceptions of atherogenesis, of the innate and adaptive immune systems, and of the participation of the latter in atherogenesis, with particular emphasis on studies of the involvement of the immune system in atherosclerosis reported in the last 2 years. This is followed by a short outline of the eight reviews that will make up this thematic series. The overview is concluded with some caveats that should be considered in the analysis of atherosclerosis in experimental animals.     

Parasite resistance and parasite tolerance: insights into transgenerational immune priming in an invertebrate host

Parasites impose different selection regimes on their hosts, which respond by increasing their resistance and/or tolerance. Parental challenge with parasites can enhance the immune response of their offspring, a phenomenon documented in invertebrates and termed transgenerational immune priming. We exposed two parental generations of the model organism Daphnia magna to the horizontally transmitted parasitic yeast Metschnikowia bicuspidata and recorded resistance- and tolerance-related traits in the offspring generation. We hypothesized that parentally primed offspring will increase either their resistance or their tolerance to the parasite. Our susceptibility assays revealed no impact of parental exposure on offspring resistance. Nonetheless, different fitness-related traits, which are indicative of tolerance, were altered. Specifically, maternal priming increased offspring production and decreased survival. Grandmaternal priming positively affected age at first reproduction and negatively affected brood size at first reproduction. Interestingly, both maternal and grandmaternal priming significantly reduced within-host–parasite proliferation. Nevertheless, Daphnia primed for two consecutive generations had no competitive advantage in comparison to unprimed ones, implying additive maternal and grandmaternal effects. Our findings do not support evidence of transgenerational immune priming from bacterial infections in the same host species, thus, emphasizing that transgenerational immune responses may not be consistent even within the same host species.     

An indirect approach to imply trade-off shapes: population level patterns in resistance suggest a decreasingly costly resistance mechanism in a model insect system

Trade-offs between life history and other traits play a key role in shaping the evolution of individuals. It is well established theoretically that the shapes of trade-off curves are as crucial to the evolutionary outcome as their strengths. However, measuring the shape of these relationships directly is often impractical. Here we use an indirect approach that examines the patterns seen within a population and then use theory to infer the shape of the trade-off curve. Using a bioassay we found that most individuals had either high susceptibility or relatively high resistance to a microparasite in a lepidopteran host population. According to general theory, this type of pattern in resistance would be most likely with a deceleratingly costly impact on fitness of increasing resistance. The implications and generality of the approach are discussed, along with the implications of the results to our understanding of the nature of innate resistance to parasites.     

Evolution of the immune system in humans from infancy to old age

This article reviews the development of the immune response through neonatal, infant and adult life, including pregnancy, ending with the decline in old age. A picture emerges of a child born with an immature, innate and adaptive immune system, which matures and acquires memory as he or she grows. It then goes into decline in old age. These changes are considered alongside the risks of different types of infection, autoimmune disease and malignancy.     

How to separate genetic and environmental causes of similarity between relatives

Related individuals often have similar phenotypes, but this similarity may be due to the effects of shared environments as much as to the effects of shared genes. We consider here alternative approaches to separating the relative contributions of these two sources to phenotypic covariances, comparing experimental approaches such as cross-fostering, traditional statistical techniques and more complex statistical models, specifically the 'animal model'. Using both simulation studies and empirical data from wild populations, we demonstrate the ability of the animal model to reduce bias due to shared environment effects such as maternal or brood effects, especially where pedigrees contain multiple generations and immigration rates are low. However, where common environment effects are strong, a combination of both cross-fostering and an animal model provides the best way to avoid bias. We illustrate ways of partitioning phenotypic variance into components of additive genetic, maternal genetic, maternal environment, common environment, permanent environment and temporal effects, but also show how substantial confounding between these different effects may occur. Whilst the flexibility of the mixed model approach is extremely useful for incorporating the spatial, temporal and social heterogeneity typical of natural populations, the advantages will inevitably be restricted by the quality of pedigree information and care needs to be taken in specifying models that are appropriate to the data.     

Investigating the genetic and environmental architecture of interpack aggression in North American grey wolves

Aggression confers several fitness benefits including increased breeding opportunities and resource acquisition. Determining the relative contributions of genetic and environmental components to shaping aggression is essential for advancing our understanding of how selection affects the distribution of aggressive phenotypes in a population. In a From the Cover article in this issue of Molecular Ecology, vonHoldt et al. (2020) used RAD‐seq methods to obtain genome‐wide single nucleotide polymorphism (SNP) data to estimate heritability of interpack aggression of 141 North American grey wolves (Canis lupus) surveyed from 1995–2018. The authors inferred heritability using both a SNP‐based genetic relationship matrix (GRM) and a consensus pedigree informed by: (a) previously obtained microsatellite data; (b) past observations of parentage; and (c) statistical reconstruction of parent‐offspring pairs. SNP‐based (i.e., GRM) and pedigree‐based (i.e., consensus pedigree) heritability estimates were 37% and 14%, respectively, with an additional 14%–16% explained by natal pack effects. The study confirmed the previously discovered strong effects of relative pack size and breeding status on interpack aggression, illustrating how social dynamics and density‐dependent factors induce variance in aggressive behaviours. Finally, the authors found associations between average individual aggression scores (IAS) and specific candidate genes (MY09A and TRAK1). In sum, vonHoldt et al. (2020) provides an unprecedented and nuanced synthesis that not only suggests gene‐aggression associations, but also emphasizes how additive genetic variance and density‐dependent factors interact to maintain phenotypic variance in aggression over time.     

昆虫免疫识别与病原物免疫逃避机理研究进展

昆虫在长期进化过程中形成复杂的天然免疫系统,病原识别是启动下游免疫反应的第一步,这一过程主要是由不同的模式识别蛋白来完成的。目前发现并鉴定的昆虫模式识别蛋白主要包括肽聚糖识别蛋白、类免疫球蛋白、β-1,3-葡聚糖结合蛋白、C型凝集素及具多功能的载脂蛋白等,不同的蛋白种类具有不同的结构、功能及识别对象。与昆虫免疫识别相对应的是,不同昆虫病原物在进化过程中发展出不同策略的免疫逃避能力,以战胜宿主免疫而致病或最终杀死昆虫。本文就昆虫免疫过程中不同模式识别蛋白的结合对象、结构与功能,以及逐渐兴起的病原物通过分子伪装等进行免疫逃避的研究进展进行了综述。并在此基础上,作者就昆虫免疫与昆虫病理研究的发展方向进行了展望,认为只有当两方面研究相结合时,才能更好地揭示昆虫宿主与病原物之间免疫与抗免疫的动态相互作用过程。     

Mass‐dependent reproductive strategies in wild bighorn ewes: a quantitative genetic approach

In the Ram Mountain bighorn sheep (Ovis canadensis) population, ewes differing by more than 30% in body mass weaned lambs with an average mass difference of only 3%. Variability in adult body mass was partly due to additive genetic effects, but inheritance of weaning mass was weak. Maternal effects could obscure genetic effects in the phenotypic expression of weaning mass, particularly if they reflected strategies of maternal expenditure that varied according to ewe mass. We performed a quantitative genetic analysis to assess genetic and environmental influences on ewe mass and on maternal expenditure. We used the mean daughters/mother regression method and Derivative Free Restricted Maximum Likelihood models to estimate heritability (h²) of ewe mass and indices of maternal expenditure. We found additive genetic effects on phenotypic variation in maternal mass, in lamb mass at weaning (absolute maternal expenditure) and in weaning mass relative to maternal mass at weaning (relative maternal expenditure). Heritability suggests that maternal expenditure has the potential to evolve. The genetic correlation of ewe mass and absolute maternal expenditure was weak, while ewe mass and relative maternal expenditure were strongly negatively correlated. These results suggest additive genetic effects on mass‐dependent reproductive strategies in bighorn ewes. Mass‐dependent reproductive strategies could affect lamb survival and phenotypic variation in adult mass. As population density increased and reproduction became costlier, small females reduced maternal expenditure more than large females. Constraints on reproductive strategy imposed by variations in resource availability are therefore likely to differ according to ewe mass. A general trend for a decrease in maternal expenditure relative to maternal size in mammals suggests that size‐dependent negative maternal effects may be common.     

Low heritabilities, but genetic and maternal correlations between red squirrel behaviours

Consistent individual differences in behaviour, and behavioural correlations within and across contexts, are referred to as animal personalities. These patterns of variation have been identified in many animal taxa and are likely to have important ecological and evolutionary consequences. Despite their importance, genetic and environmental sources of variation in personalities have rarely been characterized in wild populations. We used a Bayesian animal model approach to estimate genetic parameters for aggression, activity and docility in North American red squirrels (Tamiasciurus hudsonicus). We found support for low heritabilities (0.08-0.12), and cohort effects (0.07-0.09), as well as low to moderate maternal effects (0.07-0.15) and permanent environmental effects (0.08-0.16). Finally, we found evidence of a substantial positive genetic correlation (0.68) and maternal effects correlation (0.58) between activity and aggression providing evidence of genetically based behavioural correlations in red squirrels. These results provide evidence for the presence of heritable variation in red squirrel behaviour, but also emphasize the role of other sources of variation, including maternal effects, in shaping patterns of variation and covariation in behavioural traits.     

Environmental stress correlates with increases in both genetic and residual variances: A meta‐analysis of animal studies

Adaptive evolutionary responses are determined by the strength of selection and amount of genetic variation within traits, however, both are known to vary across environmental conditions. As selection is generally expected to be strongest under stressful conditions, understanding how the expression of genetic variation changes across stressful and benign environmental conditions is crucial for predicting the rate of adaptive change. Although theory generally predicts increased genetic variation under stress, previous syntheses of the field have found limited support for this notion. These studies have focused on heritability, which is dependent on other environmentally sensitive, but nongenetic, sources of variation. Here, we aim to complement these studies with a meta‐analysis in which we examine changes in coefficient of variation (CV) in maternal, genetic, and residual variances across stressful and benign conditions. Confirming previous analyses, we did not find any clear direction in how heritability changes across stressful and benign conditions. However, when analyzing CV, we found higher genetic and residual variance under highly stressful conditions in life‐history traits but not in morphological traits. Our findings are of broad significance to contemporary evolution suggesting that rapid evolutionary adaptive response may be mediated by increased evolutionary potential in stressed populations.     

Effects of male genetic contribution and paternal investment to egg and hatchling size in the cricket,Gryllus firmus

Egg provisions represent the complete energy supply of oviparous organisms from fertilization until hatching, and egg size is generally correlated with initial offspring size and a suite of other early fitness related traits. Since egg size is determined by the mother, little attention has been given to potential sources of paternal effects on either egg size or initial offspring size. This study considers two processes by which the sire can affect the egg size and/or initial body size of his offspring, in the multiply mated cricket, Gryllus firmus. The first is a paternal genetic effect, whereby differences in offspring genotype result in differences in the efficiency of metabolising available resources. The second is a paternal environmental effect, whereby the quality or size of paternal investment varies among male phenotypes and this is correlated with the size of eggs the females subsequently produce. Using a one-locus two-allele recessive mutation for pale eye colour as a marker, a mating experiment was designed which enabled the discrimination between eggs fertilized by two males mated simultaneously to a single female. The results of this experiment suggest that sire effects on egg and initial body size occur through both processes. Eggs fertilised by the two males were significantly different at day ten of development, suggesting that the genetic contribution of the sire is affecting embryonic body size. Further, a negative correlation was found between the head size of the pale eyed male and the size of all the eggs that the female laid, suggesting an effect of male size of the amount of nutrients the female receives from her mates. The results of this study suggest that paternal effects may be both more common and more profound than previously thought, and that studies examining early fitness traits that are correlated to egg size or initial body size, in oviparous animals, should consider the possibility and importance of the paternal contribution.     

The influences of host plant and genetic resistance to Bacillus thuringiensis on trade-offs between offspring number and growth rate in cabbage loopers, Trichoplusia ni

Abstract.  1. Variation in progeny size and quality is common among insects and this variation can strongly influence individual fitness. Larger progeny typically survive better and develop faster under adverse conditions and may have higher fecundity. Due to resource limitations, however, trade-offs may arise between having fewer large offspring or more smaller ones.
2. For cabbage loopers, Trichoplusia ni , pepper leaves are a poorer larval host than cucumber or tomato leaves as indicated by survival, development rate, and body size. Moths reared on cucumber produced more slower growing offspring than those that had been reared on pepper, which produced fewer, faster growing progeny.
3. Traits conferring resistance to Bacillus thuringiensis ( Bt ) generally are associated with strong deleterious effects that may influence resource allocation and reproductive trade-offs between progeny size and number.
4. Unlike the host-plant related trade-off between progeny size and fecundity observed among susceptible control moths, Bt -resistant parents had both the lowest fecundity and smallest progeny size on all host plants. This finding suggests that the progeny size–number relationship is constrained in resistant individuals.     

Early maternal effects and antibacterial immune factors in the eggs,nestlings and adults of the barn swallow

Transfer of immune factors via the egg may represent a maternal adaptation enhancing offspring survival. Lysozyme is a major component of maternal antibacterial immunity which is transferred to the eggs in birds. In a population of barn swallows (Hirundo rustica), lysozyme activity declined during the prelaying and laying periods in females but not in males. Egg hatching failure decreased with maternal lysozyme activity. The first eggs in a clutch contained more lysozyme and produced nestlings with larger lysozyme activity when 5 days old than last‐laid ones. In a cross‐fostering experiment where brood size was manipulated, nestling origin but not post‐manipulation brood size affected lysozyme activity. Hence, maternal lysozyme varies during the breeding season and may differentially enhance antibacterial immune defence of the eggs and nestlings in relation to laying order. These findings suggest that offspring innate immunity is influenced by early maternal effects.     

Rapid induction of immune density-dependent prophylaxis in adult social insects

The innate immune system provides defence against parasites and pathogens. This defence comes at a cost, suggesting that immune function should exhibit plasticity in response to variation in environmental threats. Density-dependent prophylaxis (DDP) has been demonstrated mostly in phase-polyphenic insects, where larval group size determines levels of immune function in either adults or later larval instars. Social insects exhibit extreme sociality, but DDP has been suggested to be absent from these ecologically dominant taxa. Here we show that adult bumble-bee workers (Bombus terrestris) exhibit rapid plasticity in their immune function in response to social context. These results suggest that DDP does not depend upon larval conditions, and is likely to be a widespread and labile response to rapidly changing conditions in adult insect populations. This has obvious ramifications for experimental analysis of immune function in insects, and serious implications for our understanding of the epidemiology and impact of pathogens and parasites in spatially structured adult insect populations.