Natural selection drives the fine-scale divergence of a coevolutionary arms race involving a long-mouthed weevil and its obligate host plant

Background

One of the major recent advances in evolutionary biology is the recognition that evolutionary interactions between species are substantially differentiated among geographic populations. To date, several authors have revealed natural selection pressures mediating the geographically-divergent processes of coevolution. How local, then, is the geographic structuring of natural selection in coevolutionary systems?

Results

I examined the spatial scale of a "geographic selection mosaic," focusing on a system involving a seed-predatory insect, the camellia weevil (Curculio camelliae), and its host plant, the Japanese camellia (Camellia japonica). In this system, female weevils excavate camellia fruits with their extremely-long mouthparts to lay eggs into seeds, while camellia seeds are protected by thick pericarps. Quantitative evaluation of natural selection demonstrated that thicker camellia pericarps are significantly favored in some, but not all, populations within a small island (Yakushima Island, Japan; diameter ca. 30 km). At the extreme, camellia populations separated by only several kilometers were subject to different selection pressures. Interestingly, in a population with the thickest pericarps, camellia individuals with intermediate pericarp thickness had relatively high fitness when the potential costs of producing thick pericarps were considered. Also importantly, some parameters of the weevil - camellia interaction such as the severity of seed infestation showed clines along temperature, suggesting the effects of climate on the fine-scale geographic differentiation of the coevolutionary processes.

Conclusion

These results show that natural selection can drive the geographic differentiation of interspecific interactions at surprisingly small spatial scales. Future studies should reveal the evolutionary/ecological outcomes of the "fine scale geographic mosaics" in biological communities.     

Metapopulation structure of a seed-predator weevil and its host plant in arms race coevolution

Although the importance of gene flow in the geographic structuring of host-parasite interactions has been well discussed, little is known about how dispersal drives the spatial dynamics of other types of coevolutionary interactions in nature. We evaluated the roles of gene flow in the geographically structured processes of a predator-prey arms race involving a seed-predatory weevil with a long mouthpart and its host camellia plant with a thick fruit coat. Molecular genetic analyses showed that both weevil and camellia populations were structured at a spatial scale of several kilometers. Importantly, the spatial pattern of the migration of weevils, but not that of camellias, imposed significant effects on the geographic configuration of the levels of coevolutionary escalation. This result suggests that even if migration is limited in one species (camellia), local coevolution with the other species that migrates between neighboring localities (weevil) can reduce the interpopulation difference in the local adaptive optima of the former species. Thus, gene flow of a species potentially homogenizes the local biological environments provided by the species and thereby promotes the evolutionary convergence of its coevolving counterparts. Consequently, by focusing on coevolutionary interactions in natural communities, "indirect" effects of gene flow on the adaptive divergence of organisms could be identified.     

Serine proteinase inhibitors from nematodes and the arms race between host and pathogen

Serine proteinase inhibitors are encoded by a large gene family of long evolutionary standing. Recent discoveries of parasite proteins that inhibit human serine proteinases, together with the complete genomic sequence from Caenorhabditis elegans, have provided a set of new serine proteinase inhibitors from more primitive metazoan animals such as nematodes. The structural features (e.g. reactive centre residues), gene organization (including intron arrangements) and inhibitory function and targets (e.g. inflammatory and coagulation pathway proteinase) all contribute important new insights into proteinase inhibitor evolution. Some parasite products have evolved that block enzymes in the mammalian host, but the human host responds with a significant immune response to the parasite inhibitors. Thus, infection produces a finely balanced conflict between host and pathogen at the molecular level, and this might have accelerated the evolution of these proteins in parasitic species as well as their hosts.     

A molecular arms race between host innate antiviral response and emerging human coronaviruses

Coronaviruses have been closely related with mankind for thousands of years. Communityacquired human coronaviruses have long been recognized to cause common cold. However, zoonotic coronaviruses are now becoming more a global concern with the discovery of highly pathogenic severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) coronaviruses causing severe respiratory diseases. Infections by these emerging human coronaviruses are characterized by less robust interferon production. Treatment of patients with recombinant interferon regimen promises beneficial outcomes, suggesting that compromised interferon expression might contribute at least partially to the severity of disease. The mechanisms by which coronaviruses evade host innate antiviral response are under intense investigations. This review focuses on the fierce arms race between host innate antiviral immunity and emerging human coronaviruses. Particularly, the host pathogen recognition receptors and the signal transduction pathways to mount an effective antiviral response against SARS and MERS coronavirus infection are discussed. On the other hand, the counter-measures evolved by SARS and MERS coronaviruses to circumvent host defense are also dissected. With a better understanding of the dynamic interaction between host and coronaviruses, it is hoped that insights on the pathogenesis of newly-identified highly pathogenic human coronaviruses and new strategies in antiviral development can be derived.

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Micro-evolutionary change and population dynamics of a brood parasite and its primary host: the intermittent arms race hypothesis

A long-term study of the interactions between a brood parasite, the great spotted cuckoo Clamator glandarius, and its primary host the magpie Pica pica, demonstrated local changes in the distribution of both magpies and cuckoos and a rapid increase of rejection of both mimetic and non-mimetic model eggs by the host. In rich areas, magpies improved three of their defensive mechanisms: nest density and breeding synchrony increased dramatically and rejection rate of cuckoo eggs increased more slowly. A stepwise multiple regression analysis showed that parasitism rate decreased as host density increased and cuckoo density decreased. A logistic regression analysis indicated that the probability of changes in magpie nest density in the study plots was significantly affected by the density of magpie nests during the previous year (positively) and the rejection rate of mimetic model eggs (negatively). These results are consistent with a hypothesis (the intermittent arms race hypothesis) of spatially structured cyclic changes in parasitism. During periods of parasitism, host defences continuously improve, and as a consequence, the fitness gains for parasites decrease. When host defences against parasites reach a high level, dispersing parasites have a selective advantage if they are able to emigrate to areas of low resistance. Once parasites have left an area hosts will lose their defensive adaptations due to their cost in the absence of parasitism. The scene is then set for re-colonization by great spotted cuckoos. Received: 7 May 1998 / Accepted: 24 August 1998     

A coevolutionary conundrum: the arms race between Diuraphis noxia (Kurdjumov) a specialist pest and its host Triticum aestivum (L.)

Aphids seemingly hold the competitive edge above plants in their arms race because of their long evolutionary time and standing association with endosymbionts. However, the advent of modern crop biotechnology has added a further component to the plant’s adaptive arsenal. In specialist associations, as in the case of Diuraphis noxia with its limited host range, both partners in the association exert innovative strategies during the macroevolutionary process that leads to the development of novel adaptive traits. In the current review, the concept of an uneven enigmatic arms race between the insect pest and its host is being argued. Many intricacies at play in the association are highlighted and adaptive strategies discussed, which may provide opportunities for either partner in the association to overcome the others’ barriers during their interaction.     

Adaptive molecular evolution for 13,000 phage generations: a possible arms race

Bacteriophage phiX174 was evolved on a continuous supply of sensitive hosts for 180 days ( approximately 13,000 phage generations). The average rate of nucleotide substitution was nearly 0.2% (11 substitutions)/20 days, and, surprisingly, substitutions accumulated in a clock-like manner throughout the study, except for a low rate during the first 20 days. Rates of silent and missense substitutions varied over time and among genes. Approximately 40% of the 71 missense changes and 25% of the 58 silent changes have been observed in previous adaptations; the rate of parallel substitution was highest in the early phase of the evolution, but 7% of the later changes had evolved in previous studies of much shorter duration. Several lines of evidence suggest that most of the changes were adaptive, even many of the silent substitutions. The sustained, high rate of adaptive evolution for 180 days defies a model of adaptation to a constant environment. We instead suggest that continuing molecular evolution reflects a potentially indefinite arms race, stemming from high levels of co-infection and the resulting conflict among genomes competing within the same cell.     

Structural insights into the arms race between host and virus along RNA silencing pathways in Arabidopsis thaliana

RNA silencing refers to a conserved sequence‐specific gene‐regulation mechanism mediated by small RNA molecules. In plants, microRNA (miRNA) and small interfering RNA (siRNA) represent two major types of small RNA molecules which play pivotal roles in plant developmental control and antiviral defences. To escape these plant defences, plant viruses have encoded a vast array of viral suppressors of RNA silencing (VSRs) to attack the host antiviral silencing pathway by interfering with small RNA processing, RNA‐induced silencing complex (RISC) assembly, viral mRNA cleavage etc. Transgenic plants expressing distinct VSRs often show developmental aberrations that resemble the phenotype of miRNA‐deficient mutants, implying a potential intrinsic link between VSRs and the miRNA pathway (at least in Arabidopsis thaliana) even though their pathogenic mechanisms remain largely unknown. In this review, we summarise our current structural understandings of the arms race between the host and virus along the RNA silencing pathway in A. thaliana by focusing on several important ribonucleoprotein (RNP) structures involved in RNA silencing and unique structural features adopted by VSRs.     

The arms race between tomato and Fusarium oxysporum

The interaction between tomato and Fusarium oxysporum f. sp. lycopersici has become a model system for the study of the molecular basis of disease resistance and susceptibility. Gene-for-gene interactions in this system have provided the basis for the development of tomato cultivars resistant to Fusarium wilt disease. Over the last 6 years, new insights into the molecular basis of these gene-for-gene interactions have been obtained. Highlights are the identification of three avirulence genes in F. oxysporum f. sp. lycopersici and the development of a molecular switch model for I-2, a nucleotide-binding and leucine-rich repeat-type resistance protein which mediates the recognition of the Avr2 protein. We summarize these findings here and present possible scenarios for the ongoing molecular arms race between tomato and F. oxysporum f. sp. lycopersici in both nature and agriculture.     

Pollination niche overlap between a parasitic plant and its host

Niche theory predicts that species which share resources should evolve strategies to minimise competition for those resources, or the less competitive species would be extirpated. Some plant species are constrained to co-occur, for example parasitic plants and their hosts, and may overlap in their pollination niche if they flower at the same time and attract the same pollinators. Using field observations and experiments between 1996 and 2006, we tested a series of hypotheses regarding pollination niche overlap between a specialist parasitic plant Orobanche elatior (Orobanchaceae) and its host Centaurea scabiosa (Asteraceae). These species flower more or less at the same time, with some year-to-year variation. The host is pollinated by a diverse range of insects, which vary in their effectiveness, whilst the parasite is pollinated by a single species of bumblebee, Bombus pascuorum, which is also an effective pollinator of the host plant. The two species therefore have partially overlapping pollination niches. These niches are not finely subdivided by differential pollen placement, or by diurnal segregation of the niches. We therefore found no evidence of character displacement within the pollination niches of these species, possibly because pollinators are not a limiting resource for these plants. Direct observation of pollinator movements, coupled with experimental manipulations of host plant inflorescence density, showed that Bombus pascuorum only rarely moves between inflorescences of the host and the parasite and therefore the presence of one plant is unlikely to be facilitating pollination in the other. This is the first detailed examination of pollination niche overlap in a plant parasite system and we suggest avenues for future research in relation to pollination and other shared interactions between parasitic plants and their hosts.     

Non-parallel morphological divergence following colonization of a new host plant

Adaptation to new ecological niches is known to spur population diversification and may lead to speciation if gene flow is ceased. While adaptation to the same ecological niche is expected to be parallel, it is more difficult to predict whether selection against maladaptive hybridization in secondary sympatry results in parallel divergence also in traits that are not directly related to the ecological niches. Such parallelisms in response to selection for reproductive isolation can be identified through estimating parallelism in reproductive character displacement across different zones of secondary contact. Here, we use a host shift in the phytophagous peacock fly Tephritis conura, with both host races represented in two geographically separate areas East and West of the Baltic Sea to investigate convergence in morphological adaptations. We asked (i) if there are consistent morphological adaptations to a host plant shift and (ii) if the response to secondary sympatry with the alternate host race is parallel across contact zones. We found surprisingly low and variable, albeit significant, divergence between host races. Only one trait, the length of the female ovipositor, which serves an important function in the interaction with the hosts, was consistently different between host races. Instead, co-existence with the other host race significantly affected the degree of morphological divergence, but the divergence was largely driven by different traits in different contact zones. Thus, local stochastic fixation or reinforcement could generate trait divergence, and additional evidence is needed to conclude whether divergence is locally adaptive.

     

Fine-scale local adaptation of weevil mouthpart length and camellia pericarp thickness: altitudinal gradient of a putative arms race

Although coevolutionary theory predicts that evolutionary interactions between species are spatially hierarchical, few studies have examined coevolutionary processes at multiple spatial scales. In an antagonistic system involving a plant, the Japanese camellia (Camellia japonica), and its obligate seed predator, the camellia weevil (Curculio camelliae), I elucidated the local adaptation of a camellia defensive armament (pericarp thickness) and a weevil offensive armament (rostrum length) within Yakushima Island (ca. 30 km in diameter), compared to a larger-scale variation in those traits throughout Japan reported in previous studies. Results showed that camellia pericarp thickness and weevil rostrum length vary remarkably within several kilometers on this island. In addition, geographic variation in each camellia and weevil armament was best explained by the armament size of the sympatric participant than by abiotic environmental heterogeneity. However, I also found that camellia pericarp thickness significantly decreased in cool-temperate (i.e., highland) areas, suggesting the contributions of climate on the spatial structuring of the weevil-camellia interaction. Interestingly, relatively thin pericarps occurred not only in the highlands but also in some low-altitude areas, indicating that other factors such as nonrandom or asymmetric gene flow play important roles in the metapopulation processes of interspecific interactions at small spatial scales.     

Adaptation to different host plant ages facilitates insect divergence without a host shift

Host shifts and subsequent adaption to novel host plants are important drivers of speciation among phytophagous insects. However, there is considerably less evidence for host plant-mediated speciation in the absence of a host shift. Here, we investigated divergence of two sympatric sister elm leaf beetles, Pyrrhalta maculicollis and P. aenescens, which feed on different age classes of the elm Ulmus pumila L. (seedling versus adult trees). Using a field survey coupled with preference and performance trials, we show that these beetle species are highly divergent in both feeding and oviposition preference and specialize on either seedling or adult stages of their host plant. An experiment using artificial leaf discs painted with leaf surface wax extracts showed that host plant chemistry is a critical element that shapes preference. Specialization appears to be driven by adaptive divergence as there was also evidence of divergent selection; beetles had significantly higher survival and fecundity when reared on their natal host plant age class. Together, the results identify the first probable example of divergence induced by host plant age, thus extending how phytophagous insects might diversify in the absence of host shifts.     

Reciprocal selection causes a coevolutionary arms race between crossbills and lodgepole pine

Few studies have shown both reciprocal selection and reciprocal adaptations for a coevolving system in the wild. The goal of our study was to determine whether the patterns of selection on Rocky Mountain lodgepole pine (Pinus contorta spp. latifolia) and red crossbills (Loxia curvirostra complex) were concordant with earlier published evidence of reciprocal adaptations in lodgepole pine and crossbills on isolated mountain ranges in the absence of red squirrels (Tamiasciurus hudsonicus). We found that selection (directional) by crossbills on lodgepole pine where Tamiasciurus are absent was divergent from the selection (directional) exerted by Tamiasciurus on lodgepole pine. This resulted in divergent selection between areas with and without Tamiasciurus that was congruent with the geographic patterns of cone variation. In the South Hills, Idaho, where Tamiasciurus are absent and red crossbills are thought to be coevolving with lodgepole pine, crossbills experienced stabilizing selection on bill size, with cone structure as the agent of selection. These results show that crossbills and lodgepole pine exhibit reciprocal adaptations in response to reciprocal selection, and they provide insight into the traits mediating and responding to selection in a coevolutionary arms race.     

Geographic divergence in the relationship between Paragobiodon echinocephalus and its obligate coral host

The redhead goby Paragobiodon echinocephalus lives exclusively within the branching coral Stylophora pistillata . While in the Great Barrier Reef fish occupation rate of large coral is higher than that of small coral, an opposite pattern exists in the northern Red Sea. It is suggested that this pattern is caused by a limitation on the adult body size of fish in the northern Red Sea.     

A chemical level in the coevolutionary arms race between an ant social parasite and its hosts

Here we investigate the coevolutionary interactions between the slavemaking ant Protomognathus americanus and its Temnothorax hosts on a chemical level. We show that, although this social parasite is principally well-adapted to its hosts' cuticular hydrocarbon profile, there are pronounced differences in the fine-tuning of this adaptation. Between populations, chemical adaptation varies with host community composition, as the parasite faces a trade-off when confronted with more than one host species. In addition to adaptation of its own chemical signature, the slavemaker causes a reciprocal adjustment in its slaves' cuticular profile, the degree of which depends on the slave species. On the host side, successful parasite defence requires efficient enemy recognition, and in behavioural aggression trials, host colonies could indeed discriminate between invading slaves, which commonly accompany slavemakers on raids, and free-living conspecifics. Furthermore, hosts shifted their acceptance threshold over the seasons, presumably to reduce the costs of defence.