The evolution of immune defense and song complexity in birds

Abstract There are three main hypotheses that explain how the evolution of parasite virulence could be linked to the evolution of secondary sexual traits, such as bird song. First, as Hamilton and Zuk proposed a role for parasites in sexual selection, female preference for healthy males in heavily parasitized species may result in extravagant trait expression. Second, a reverse causal mechanism may act, if sexual selection affects the coevolutionary dynamics of host-parasite interactions per se by selecting for increased virulence. Third, the immuno-suppressive effects of ornamentation by testosterone or limited resources may lead to increased susceptibility to parasites in species with elaborate songs. Assuming a coevolutionary relationship between parasite virulence and host investment in immune defense we used measures of immune function and song complexity to test these hypotheses in a comparative study of passerine birds. Under the first two hypotheses we predicted avian song complexity to be positively related to immune defense among species, whereas this relationship was expected to be negative if immuno-suppression was at work. We found that adult T-cell mediated immune response and the relative size of the bursa of Fabricius were independently positively correlated with a measure of song complexity, even when potentially confounding variables were held constant. Nestling T-cell response was not related to song complexity, probably reflecting age-dependent selective pressures on host immune defense. Our results are consistent with the hypotheses that predict a positive relationship between song complexity and immune function, thus indicating a role for parasites in sexual selection. Different components of the immune system may have been independently involved in this process.     

Dynamic optimization of host defense, immune memory, and post-infection pathogen levels in mammals

When attacked by pathogens, higher vertebrates produce specific immune cells that fight against them. We here studied the host's optimal schedule of specific immune cell production. The damage caused by the pathogen increases with the pathogen amount in the host integrated over time. On the other hand, there is also a cost incurred by the production of specific immune cells, not only in terms of the energy needed to produce and maintain the cells, but also with respect to damages sustained by the host's body as a result of immune activity. The optimal strategy of the host is the one that minimizes the total cost, defined as a weighted sum of the damage caused by pathogens and the costs caused by the specific immune cells. The problem is solved by using Pontryagin's maximum principle and dynamic programming. The optimal defense schedule is typically as follows: In the initial phase after infection, immune cells are produced at the fastest possible rate. The amount of pathogen increases temporarily but is eventually suppressed. When the pathogen amount is suppressed to a sufficiently low level, the immune cell number decreases and converges to a low steady level, which is maintained by alternately switching between fastest production and no production. We examine the effect of time delay required to have fully active immune cells by comparing cases with different number of rate limiting steps before producing immune cells. We examine the effect of the duration of time (time delay) required before full-scale production of active immune cells by comparing cases with different numbers of rate-limiting steps before immune-cell production. We also discuss the role of immune memory based on the results of the optimal immune reaction.     

植物防御反应与动物免疫应答的比较及其对应性初探

动物经过数亿年的进化直到脊椎动物阶段出现了渐为完整的免疫系统。植物在与各种病原的共进化过程中亦发展了自身的防御系统。随着对植物抗病性的概念及植物防御机制的不断认识,人们发现它与动物的免疫应答有着众多的对应性。这些对应性是否表明植物的防御系统与动物的免疫系统在进化上具有同一性,是否表明它们在防御反应上具有类似的机制值得深思 。     

Temporal dynamics of a T-cell mediated immune response in desert rodents

Immunocompetence, the general capacity of an individual host to mount an immune response against pathogens, is commonly assessed by the response to a challenge of the immune system by injection of phytohaemagglutinin (PHA). The response to PHA is commonly considered a reliable estimate of the T-cell mediated immune response. We investigated the temporal pattern of the PHA response in 10 rodent species from the Negev desert, Israel. We hypothesized that the temporal dynamics of the PHA response would differ among species with different natural patterns of flea parasitism. We injected PHA subcutaneously in the footpad of each rodent and measured its PHA response 6, 24 and 48 h after injection. Rodent species showed two types of PHA response. One type was rapid and characteristic of rodents that had either species-poor flea assemblages, or that are rarely attacked by fleas. This response peaked approximately 6 h after PHA injection. The second type of response was delayed and was typical of rodents that have either species-rich flea assemblages or high abundance and prevalence of fleas or both. Their response to PHA peaked 24 h after injection. Furthermore, rodents that responded promptly had a lower maximum response than rodents with a delayed response. Our results suggest the occurrence of a trade-off between intensity and latency of the PHA response and, therefore, the necessity to account for the relationship between maximum PHA response and time after injection when making interspecific comparisons of immunocompetence.     

Two arms are better than one: parasite variation leads to combined inducible and constitutive innate immune responses

Parasites represent a major threat to all organisms which has led to the evolution of an array of complex and effective defence mechanisms. Common to both vertebrates and invertebrates are innate immune mechanisms that can be either constitutively expressed or induced on exposure to infection. In nature, we find that a combination of both induced and constitutive responses are employed by vertebrates, invertebrates and, to an extent, plants when they are exposed to a parasite. Here we use a simple within-host model motivated by the insect immune system, consisting of both constitutive and induced responses, to address the question of why both types of response are maintained so ubiquitously. Generally, induced responses are thought to be advantageous because they are only used when required but are too costly to maintain constantly, while constitutive responses are advantageous because they are always ready to act. However, using a simple cost function but with no a priori assumptions about relative costs, we show that variability in parasite growth rates selects for a strategy that combines both constitutive and induced defences. Differential costs are therefore not necessary to explain the adoption of both forms of defence. Clearly, hosts are likely to be challenged by variable parasites in nature and this is sufficient to explain why it is optimal to deploy both arms of the innate immune system.     

Warfare and defense: The host response to Cryptococcus infection

Cryptococcus neoformans and Cryptococcus gatti are the etiological agents of cryptococcosis, a life-threatening mycosis affecting the central nervous system. Cryptococcal meningoencephalitis is the most fatal mycosis in AIDS patients, resulting almost 200 000 deaths annually. High cost, side effects and drug resistance are constant elements during treatment of cryptococcosis, encouraging the development of novel therapeutic strategies including immunomodulatory protocols. Thereby, to understand how the host responds to Cryptococcus is essential. In this review, we discuss the immune response against Cryptococcus and immunoevasion strategies.     

Predation risk, host immune response, and parasitism

Predation risk may affect the allocation priorities of limitingresources by potential prey. Investment in immune function shouldreceive reduced priority, when hosts are exposed to predatorsbecause of the costs of immune function. We tested this hypothesisby randomly exposing adult house sparrows, Passer domesticus,to either a cat, Felis catus, or a rabbit, Oryctolagus cuniculus,for 6 h while assessing their ability to raise a T-cell–mediatedimmune response to a challenge with phytohemagglutinin. Sparrowsexposed to a cat had a significant reduction of, on average,18% and 36% in T-cell response in two different experimentscompared with sparrows that were exposed to a rabbit. In a fieldexperiment with a barn owl, Tyto alba, or a rock dove, Columbalivia, placed next to a nest-box during laying, we found a meanreduction in T-cell–mediated immune response of 20%. Inmales, the reduction in cell-mediated immune response owingto cat exposure increased with increasing size of the badge,which is a secondary sexual character, but only during the breedingseason. In a third experiment, house sparrows were either exposedto a barn own, T. alba, or a rock dove, C. livia, and developmentof malarial infections was recorded during the following 6 weeks.Individual sparrows exposed to a predator had a higher prevalenceand intensity of Haemoproteus malarial infection than did controlindividuals. Therefore, exposure to predators reduced theirability of hosts to cope with parasitism mediated through effectson immune function.     

Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae

Due to the close association between parasites and their hosts, many ‘generalist’ parasites have a high potential to become specialized on different host species. We investigated this hypothesis for a common ectoparasite of seabirds, the tick Ixodes uriae that is often found in mixed host sites. We examined patterns of neutral genetic variation between ticks collected from Black‐legged kittiwakes (Rissa tridactyla) and Atlantic puffins (Fratercula arctica) in sympatry. To control for a potential distance effect, values were compared to differences among ticks from the same host in nearby monospecific sites. As predicted, there was higher genetic differentiation between ticks from different sympatric host species than between ticks from nearby allopatric populations of the same host species. Patterns suggesting isolation by distance were found among tick populations of each host group, but no such patterns existed between tick populations of different hosts. Overall, results suggest that host‐related selection pressures have led to the specialization of I. uriae and that host race formation may be an important diversifying mechanism in parasites.     

禽沙门菌诱导宿主免疫应答的特性

沙门菌病(Salmonellosis)是全世界最普遍的食源性疾病之一,不仅对养殖业造成经济损失,还对人类安全构成威胁。禽沙门菌感染肠道后,可诱导肠上皮细胞表达多种TLRs和炎症反应的发生,在分泌的趋化因子作用下免疫效应细胞迁移到感染部位。细菌通过肠上皮细胞屏障后被巨噬细胞或树突状细胞吞噬,其中巨噬细胞是沙门菌的主要定殖场所。天然免疫系统将抗原递呈给淋巴细胞后,机体能够在2–3周内通过以Th1为主的免疫应答清除在肠道和深层组织中的沙门菌。而宿主特异性血清型鸡白痢沙门菌从肠道侵入后,在肝脾和其他器官中定殖,进而引发全身感染。早期感染阶段不会引起肠道炎症反应,主要诱导以Th2为主的免疫应答,而Th1型应答相对较弱,有利于鸡白痢沙门菌在机体内的持续存在和感染。本文围绕禽沙门菌的致病机理和免疫应答特性进行阐述,尤其对鸡白痢沙门菌免疫逃逸和持续载菌的特性进行深入分析,为禽沙门菌病的防控提供新靶标和新见解。     

抗病毒免疫中干扰素与炎症信号通路的交互调控：防御反应与维持稳态

天然免疫是机体通过识别自身或外部危险信号后,为维持体内稳态而逐步建立起来的一系列防御反应,当宿主细胞内的模式识别受体识别胞内病原相关分子模式后激活干扰素(interferon, IFN)、核因子-kappa B (nuclear factor-kappa B, NF-κB)和炎性小体等信号通路。IFNs在天然免疫应答中发挥重要作用,它诱导的抗病毒基因能够通过多种方式抵御病毒的感染,炎症反应则是机体自动的防御反应,能够在病毒感染机体时释放促炎性细胞因子以调控机体的免疫反应,进而发挥抗病毒作用。在病毒感染过程中,IFN信号通路与炎症反应调控网络中的关键分子如NF-κB/RelA、PKR等存在一定的交互作用,此外,IFN信号通路及其产生的细胞因子又影响其他信号通路的活化,进而调控机体的免疫应答以维持自身稳态,它们之间的交互调控失衡将会引起过度炎症反应,导致组织器官的免疫病理损伤,例如SARS-CoV-2感染机体时产生的过度炎症反应。本文综述了机体抗病毒免疫过程中干扰素信号通路与炎症反应之间的交互调控,为研发抗病毒策略提供新思路。     

There and back again: switching between host orders by avian body lice (Ischnocera: Goniodidae)

Studies of major switches by parasites between highly divergent host lineages are important for understanding new opportunities for parasite diversification. One such major host switch is inferred for avian feather lice (Ischnocera) in the family Goniodidae, which parasitize two distantly‐related groups of birds: Galliformes (pheasants, quail, partridges, etc.) and Columbiformes (pigeons and doves). Although there have been several cophylogenetic studies of lice at the species level, few studies have focused on such broad evolutionary patterns and major host‐switching events. Using a phylogeny based on DNA sequences for goniodid feather lice, we investigated the direction of this major host switch. Unexpectedly, we found that goniodid feather lice have switched host orders, not just once, but twice. A primary host switch occurred from Galliformes to Columbiformes, leading to a large radiation of columbiform body lice. Subsequently, there was also a host switch from Columbiformes back to Galliformes, specifically to megapodes in the Papua–Australasian region. The results of the present study further reveal that, although morphologically diagnosable lineages are supported by molecular data, many of the existing genera are not monophyletic and a revision of generic limits is needed. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 614–625.     

Evolution of Euphilotes (Lepidoptera: Lycaenidae) by seasonal and host shifts

The lycaenid butterfly genus Euphilotes , consisting of five species and several dozen subspecies, is confined to western North America. Each subspecies utilizes one or a few species of Eriogonum (Polygonaceae) as larval hosts; larvae feed entirely on pollen and developing seeds. Euphilotes populations are (with few exceptions) univoltine and fly in synchrony with the initial (c. 2 weeks) annual flowering periods of their hosts. Euphilotes evolution coincides with shifts to new hosts, frequently with different bloom periods. Often both inter- and intraspecific populations occur in sympatry. Although interspecific populations may fly in synchrony and utilize the same hosts, sympatric intraspecific populations use different hosts and generally fly allochronically. Analyses of Euphilotes populations using biochemical, morphological, and life history characters, do not support either coevolution or sequential evolution with Eriogonum but are more consistent with opportunistic adaptation to new hosts having different bloom periods.     

Protective plant immune responses are elicited by bacterial outer membrane vesicles

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Sex differences in the protection of host immune systems by a polyembryonic parasitoid

Endoparasitoids have the ability to evade the cellular immune responses of a host and to create an environment suitable for survival of their progeny within a host. Generally, the host immune system is suppressed by endoparasitoids. However, polyembryonic endoparasitoids appear to invade their hosts using molecular mimicry rather than immune system suppression. It is not known how the host immune system is modified by polyembryonic endoparasitoids. Using haemocyte counts and measurement of cellular immune responses, we evaluated modification of the host immune system after separate infestations by a polyembryonic parasitoid (Copidosoma floridanum) and another parasitoid (Glyptapanteles pallipes) and by both together (multi-parasitism). We found that the polyembryonic parasitoid maintains and enhances the host immune system, whereas the other parasitoid strongly suppresses the immune system. Multi-parasitization analysis revealed that C. floridanum cancelled the immune suppression by G. pallipes and strengthened the host immunity. This enhancement was much stronger with male than with female C. floridanum.     

Tumour angiogenesis normalized by myo-inositol trispyrophosphate alleviates hypoxia in the microenvironment and promotes antitumor immune response

Pathologic angiogenesis directly responds to tumour hypoxia and controls the molecular/cellular composition of the tumour microenvironment, increasing both immune tolerance and stromal cooperation with tumour growth. Myo-inositol-trispyrophosphate (ITPP) provides a means to achieve stable normalization of angiogenesis. ITPP increases intratumour oxygen tension (pO₂) and stabilizes vessel normalization through activation of endothelial Phosphatase-and-Tensin-homologue (PTEN). Here, we show that the tumour reduction due to the ITPP-induced modification of the tumour microenvironment by elevating pO₂ affects the phenotype and properties of the immune infiltrate. Our main observations are as follows: a relative change in the M1 and M2 macrophage-type proportions, increased proportions of NK and CD8⁺T cells, and a reduction in Tregs and Th2 cells. We also found, in vivo and in vitro, that the impaired access of PD1⁺NK cells to tumour cells is due to their adhesion to PD-L1⁺/PD-L2⁺ endothelial cells in hypoxia. ITPP treatment strongly reduced PD-L1/PD-L2 expression on CD45+/CD31+ cells, and PD1⁺ cells were more numerous in the tumour mass. CTLA-4⁺ cell numbers were stable, but level of expression decreased. Similarly, CD47⁺ cells and expression were reduced. Consequently, angiogenesis normalization induced by ITPP is the mean to revert immunosuppression into an antitumor immune response. This brings a key adjuvant effect to improve the efficacy of chemo/radio/immunotherapeutic strategies for cancer treatment.     

Roles of IκB kinase ε in the innate immune defense and beyond

IκB kinase ε (IKKε) is a non-canonical IκB kinase that is extensively studied in the context of innate immune response. Recently, significant progress has been made in understanding the role of IKKε in interferon (IFN) signaling. In addition to its roles in innate immunity, recent studies also demonstrate that IKKε is a key regulator of the adaptive immune response. Specifically, IKKε functions as a negative feedback kinase to curtail CD8 T cell response, implying that it can be a potential therapeutic target to boost antiviral and antitumor T cell immunity. In this review, we highlight the roles of IKKε in regulating IFN signaling and T cell immunity, and discuss a few imminent questions that remain to be answered.