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Coevolution of daily activity timing in a host–parasite system
Abstract
Coevolutionary theories applied in the study of host–parasite systems indicate that lineages exhibit progressive trends in response to reciprocal selective pressures. Avian brood parasites have generated intense interest as models for coevolutionary processes. Similar to avian cuckoos, Polistes wasp social parasites usurp a nest and exploit the parental care of a congeneric species to rear their own brood. In the present study, we show a coevolutionary arms race in the daily activity pattern in a Polistes host–parasite pair. We measured the daily activity rate, in constant laboratory conditions, of both host and parasite females during the period in which nest usurpations occur. The parasites showed a hyperkinesis in the middle of the day. As the field observations suggested, this mid-day activity is used to perform host nest usurpation attempts. Timing the usurpations allows the parasite to maximize its usurpation attempts during daytime when the host defence is lower. A field comparison of host presence on the nest in two populations with different parasitism rates showed that populations under strong parasitic pressure exhibit timing counteradaptations to optimize nest defence. This study provides the first example of a mutual coadaptation in timing activity in a parasite–host system. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 399–405.
... Social parasites often evolve by breaking into and often mimicking the communication system by which host individuals recognize each other (Lenoir et al. 2001;Lorenzi 2006;Bagnères and Lorenzi 2010). Subsequent or concomitant coevolution may involve multiple other parasite and host traits (e.g., Foitzik and Herbers 2001b;Foitzik et al. 2001Foitzik et al. , 2003Foitzik et al. , 2009Ortolani andCervo 2009, 2010). The interactions are often geographically complex, because social parasites are patchily distributed (Wilson 1971), and may involve different numbers of host and social parasite species in different localities (Johnson and Herbers 2006). ...
... using calipers accurate to 0.05 mm. Head width is a reliable indicator of body size and relative fighting ability in Polistes (Eickwort 1969;Ortolani and Cervo 2009). Because colonies are annual and monogynous and each foundress is the only egg-layer in the colony, we estimated the true lifetime fitness of the foundresses as the number of pupae produced during the nesting cycle. ...
Social parasites exploit societies, rather than organisms, and rear their brood in social insect colonies at the expense of their hosts, triggering a coevolutionary process that may affect host social structure. The resulting coevolutionary trajectories may be further altered by selection imposed by predators, which exploit the abundant resources concentrated in these nests. Here, we show that geographic differences in selection imposed by predators affects the structure of selection on coevolving hosts and their social parasites. In a multiyear study, we monitored the fate of the annual breeding attempts of the solitary nesting foundresses of Polistes biglumis wasps in four geographically distinct populations that varied in levels of attack by the congeneric social parasite, P. atrimandibularis. Foundress fitness depended mostly on whether, during the long founding phase, a colony was invaded by social parasites or attacked by predators. Foundresses from each population differed in morphological traits and reproductive tactics that were consistent with selection imposed by their natural enemies and in ways that may affect host sociality. In turn, parasite traits were consistent with selection imposed locally by hosts, implying a geographic mosaic of coevolution in this brood parasitic interaction.
... Αντίθετα, λίγοι επικονιαστές απαντώνται στις σφήκες, με την οικογένεια Agaonidae να αποτελεί την σημαντικότερη ομάδα επικονιαστών των συκιών (Ficus sp.). Άλλα είδη, όπως η οικογένεια Chrysididae, κάποια είδη του γένους Polistes (Vespidae) και η υποοικογένεια Nomadinae (Apidae), δρουν ως κλεπτοπαράσιτα και γεννούν τα ωά τους είτε σε φωλιές άλλων σφηκών (Chrysididae, διάφορα Polistes) είτε σε είδη μελισσών που συλλέγουν γύρη και, αφού εκκολαφθούν, καταναλώνουν την μπάλα γύρης αλλά συχνά και το ωό που έχει τοποθετηθεί από τον ξενιστή (Nomadinae) (Dapporta et al. 2004, Ortolani & Cervo 2009). Πολλά Υμενόπτερα, όπως τα Ichneumonοidea (Ichneumonidae και Braconidae), αποτελούν σημαντικά παρασιτοειδή σε ένα ευρύ φάσμα εντόμωνξενιστών, ενώ άλλα Υμενόπτερα,όπως τα Cynipoidea, αποτελούν σημαντικά παρασιτοειδή σε ένα ευρύ φάσμα φυτώνξενιστών. ...
Lesvos is the third biggest island of Greece, part of the East Aegean Islands and located near the coastline of Anatolia peninsula. In contrast to other islands, such as Crete, Corfu, Samos and Rhodes, the island’s arthropod fauna was understudied and with many literature gaps and for this reason, extensive research was required. Samplings took place from April 2019 to January 2022 by using pitfall traps, collecting specimens by hand and collecting and isolating galls. At first, samplings with pitfall traps took place between 2nd March 2021 and 5th May 2021 from 28 sampling stations in the area of Pirgoi Thermis. In addition, arthropods were collected by hand throughout the island of Lesvos between April 2019 and January 2022. At the same time, from March 2021 to January 2022, gall samplings from various host plants took place and they were isolated in order to collect emerged adults, parasitoids and inquilines. Consequently, all collected arthropods were photographed with a camera and, then, the photos were uploaded on the online platform iNaturalist in order to fully record the place and the date of each observation. In total, 339 different arthropod species were recorded from 29 orders, from which 12 species are probably new for science and 20 species are new for Greece. Moreover, 33 alien and invasive arthropod species were collected as well as 16 endemic species. Finally, whether Lesvos is an area of endemism is under discussionas well as the value of studying the local fauna to the benefit of agriculturists, doctors and citizens.
... Indeed, defence trait expression covaries with parasite pressure from the slavemaking ant T. americanus over the geographical ranges of two Temnothorax host species [44,46,138]. A similar association between parasite presence and defence trait expression was found in Polistes wasps, where foundresses in parasitized locales have enlarged body size and are more often present on the nest during mid-day, which is when parasitic wasps are most likely to attack [33,139]. On the other hand, spatial association between parasite occurrence and defence trait expression can also be the result of induced defences following parasite contact. ...
Insect societies face many social parasites that exploit their altruistic behaviours or their resources. Due to the fitness costs these social parasites incur, hosts have evolved various behavioural, chemical, architectural and morphological defence traits. Similar to bacteria infecting multicellular hosts, social parasites have to successfully go through several steps to exploit their hosts. Here, we review how social insects try to interrupt this sequence of events. They can avoid parasite contact by choosing to nest in parasite-free locales or evade attacks by adapting their colony structure. Once social parasites attack, hosts attempt to detect them, which can be facilitated by adjustments in colony odour. If social parasites enter the nest, hosts can either aggressively defend their colony or take their young and flee. Nest structures are often shaped to prevent social parasite invasion or to safeguard host resources. Finally, if social parasites successfully establish themselves in host nests, hosts can rebel by killing the parasite brood or by reproducing in the parasites' presence. Hosts of social parasites can therefore develop multiple traits, leading to the evolution of complex defence portfolios of co-dependent traits. Social parasites can respond to these multi-level defences with counter-adaptations, potentially leading to geographical mosaics of coevolution.
This article is part of the Theo Murphy meeting issue ‘Evolution of pathogen and parasite avoidance behaviours’.
... Thirty-one usurpation trials were carried out outdoors on warm, bright days between 1300 and 1600 hours (identified by Ortolani & Cervo (2009) as the time of peak activity in a related social parasite, P. sulcifer). In each trial, a single parasite was placed in a plastic cage (34 Â 18 cm and 27 cm high) containing a target host nest and allowed to approach the nest and interact with hosts. ...
Costs associated with escalated fighting may be minimized where individuals are able to gather information regarding the likely outcome of conflicts. In particular, the ability to assess resource-holding potential (RHP) has been shown to be important in determining the dynamics of animal contests. While assessment rules have been investigated in contests in a range of species, little is known about the potential for assessment in contests between species. We examined the role of assessment in usurpation contests between the paper wasp Polistes dominulus and the social parasite Polistes semenowi. First, we investigated whether parasite clypeal patterns function as signals of RHP by staging contests with parasites in which the clypeal pattern was concealed with paint. Second, we examined the importance of body size as a determinant of RHP. Finally, we explored whether individuals use information about their own RHP, and that of their rivals, in deciding when to withdraw. We found no evidence that parasite clypeal patterns act to signal RHP to hosts: initial fights were neither longer nor more intense when the patterns were concealed. We also found no evidence for RHP assessment during contests: although body size predicted contest outcome, fight duration and intensity were not significantly related to either winner or loser size. We suggest that the high value of the nest to both parties, combined with the potential for ‘divisive’ asymmetries in RHP between hosts and parasites, may result in selection for escalated conflict over rival assessment during usurpation fights.
... Overwintering wasps bearing fertilized Xenos females may spread the infective first-instar larvae, the triungulins, while foraging on flowers (phoresy) or wandering among nests (Hughes et al. 2003) prior to the emergence of the first workers and in the middle of the day, when the queen is foraging and the nest is unprotected (Beani & Massolo 2007). This is a seasonal and daily 'undefended time window' also exploited by social parasites, that is, species that profit by the parental care of a congeneric species to rear their brood (Nannoni et al. 2001;Ortolani & Cervo 2009). To escape defensive reactions of the adult wasps, triungulins rapidly penetrate into all larval stages of Polistes, one or more per wasp larva, without any selective hostseeking behaviour (Vannini et al. 2008;Manfredini et al. 2010a). ...
The macroparasite Xenos vesparum affects both the behaviour and the physical traits of its host, the social wasp Polistes dominulus. Female wasps, if parasitized, do not perform any social tasks and desert the colony to gather at specific sites, where the parasite mates; at the end of summer they form prehibernating clusters joined by healthy future queens to overwinter. Parasitized wasps become highly gregarious. In April, healthy wasps leave the aggregations to found new colonies, while parasitized wasps remain in overwintering groups and release parasites to infect wasp larvae only later in the season. We studied the prolonged gregarious behaviour of parasitized wasps and analysed the morphology of parasitized and healthy wasps in aggregations collected over a 7-year period to determine whether the parasite affects host size, wing symmetry, ovarian development and lipid stores. All parasitized wasps were smaller and had undeveloped ovaries and more wing fluctuating asymmetry than unparasitized wasps, irrespective of time of year, parasite load and parasite sex. If infected only by one or two X. vesparum females, the wasps had large fat bodies, which could facilitate their overwintering. In contrast, wasps infected by at least one male parasite had little lipid and died at the end of the summer. Thus, X. vesparum, may play a role in the fate of its host, by exploiting wasps' tendency to form aggregations outside the colony and by altering its caste system, nutrient allocation, diapause timing and life span to achieve its own reproduction and dispersal.
... The foundresses were tested at the end of May or at the beginning of June, just before the worker emergence period. This temporal window corresponds to the period in which P. sulcifer females are searching for host colonies to usurp in the wild (Cervo & Turillazzi 1996;Ortolani & Cervo 2009). ...
Obligate social parasite insects are specialized in exploiting the parental service of the workers of another social species by invading their colonies. As social insects are usually aggressive towards intruders, social parasites have to circumvent the host’s nestmate recognition system to enter the host colony successfully. Many studies on paper wasps have shown that, after host nest invasion, Polistes social parasites change their chemical profile to match the host’s odour, thus allowing their acceptance into its colony. However, a social parasite’s usurpation strategy may benefit from signals that reduce or eliminate the aggression of the host. We used lure presentation experiments to investigate whether Polistes sulcifer, a social parasite of the paper wasp P. dominulus, is able to reduce the aggressive reaction of its host. We found that the parasite lure elicited lower host aggressiveness than the conspecific lure, suggesting that parasite species have evolved cues able to inhibit host aggressiveness. We investigated separately the effects of chemical and visual patterns on host aggressiveness. The lower host reaction to the parasite lure was not due to chemical cues, but was elicited by the visual facial pattern of the parasite. Experimental manipulation of this visual pattern demonstrated that the black lower part of the clypeus of the parasite is the trait able to reduce host aggression. This pattern can be considered an honest signal since it visually amplifies the mandibular width, giving information about the parasite’s dangerousness.
... Gregariousness -here the tendency to aggregate in confined as well as in open space -promotes the displacement of batches of infective larvae through the brood canal and could have evolved to increase parasitism success when conditions are favourable. Peaks of nest infections on the field happen during the hottest hours of the day, when most foragers are outside the nest (Ortolani & Cervo 2009): this moment corresponds also to high metabolic activity of wasp larvae (thus high production of CO 2 ) and intense light. We cannot exclude any cooperative action between sibling parasites during the infection process (Costa & Fitzgerald, 1996): a decreased risk of predation is likely to occur in group. ...
The first-instar larvae of strepsipteran parasites, commonly referred to as “triungulins”, are the host-seeking stage: they must locate, invade and successfully develop in the new host, in order to start their parasitic cycle. Little information is available about the behaviour of Xenos vesparum triungulins. They emerge in batches from the endoparasitic female infecting Polistes dominulus, the primary host, and reach the nest through a vector (a foraging wasp or the parasitised wasp itself). Once there, they have the possibility to penetrate into wasp immatures at different developmental stages. In this study, we performed preliminary analyses aimed to investigate which cues are important to direct triungulin movements during their brief stay in wasp nests. In laboratory conditions we selectively presented different stimuli to Xenos larvae: apparently, the host larva itself is attractive in an open arena, but not inside a confined space, nor are epicuticular compounds of wasp larvae able to control triungulin movements. These are more likely oriented by their gregarious behaviour, whereas light (positive phototaxy) may at a previous stage enhance their emergence via the brood canal opening in the female cephalothorax.
... Other parasites were activated during May (when usurpation usually occurs) by a 'warming treatment' (as defined in Ortolani et al. 2008, i.e. natural light:dark condition with additional light bulb from 0800 to 2000 hours, maximum temperature in the range 28e34 C). This treatment simulates the field conditions in which parasites usurp the nests (Ortolani et al. 2008; Ortolani & Cervo 2009). Then, the parasites were introduced into host colony cages and only those parasites directly approaching the nest (N ¼ 18) were considered for the chemical analyses (during the usurpation phase). ...
Insect social parasites need to overcome host colonies’ defences to exploit their resources successfully. Sophisticated sensory deception mechanisms to break the host’s barriers have been repeatedly reported for many social parasites, possibly concealing the importance of open fighting, a more ancestral strategy. Understanding the relative importance of fooling and fighting is primarily challenging when the two strategies seem both available and advantageous. We focused on the paper wasp social parasite–host system Polistes sulcifer–P. dominulus, where both fooling and fighting have been suggested to play a role during usurpation contests. Host aggression is elicited by the chemical cues (hydrocarbons) that intruders bear on their cuticle. Parasites would benefit from reducing the amount of these cues before approaching the host colony. In addition, the parasites’ facial pattern has been shown to reduce the host’s aggressive reaction, probably by amplifying the mandibular width. We tested the occurrence of chemical and visual cheating through chemical analyses and laboratory usurpation trials, respectively. Usurping parasites did not conceal their identity by reducing cuticular hydrocarbons, nor did their facial pattern facilitate nest take-over. Contest outcome was instead predicted by the relative body size of the opponents. Fighting, rather than fooling, is therefore the strategy used by P. sulcifer usurping females. The importance of physical strength could thus explain why chemical or visual tricks do not play a role in taking over the host colony despite their potential usefulness. Our findings suggest that the evolution of sophisticated cheating mechanisms can be prevented by the ability to fight.
... Parasites were then activated for a period ranging from 4 to 16 days by a 'warming treatment' [as defined previously ( Ortolani et al., 2008); i.e. natural L:D conditions with additional artificial lighting from 08.00 h to 20.00 h]. This treatment simulates the field condition during which parasites usurp the nests in the wild ( Ortolani et al., 2008;Ortolani and Cervo, 2009). Twenty colonies of P. dominulus were collected before the emergence of workers in early spring (April) in the area around Florence (Central Italy). ...
Insect social life is governed by chemicals. A great number of studies have demonstrated that the blend of hydrocarbons present on the cuticle (CHCs) plays a pivotal role in intra- and inter-specific communication. It is not surprising, therefore, that social parasites, specialized in exploiting the costly parental care provided by host workers, exploit the host chemical communication system too. Throughout their life cycle, social parasites intercept and break this CHC-based code. Recently, however, several polar compounds (mainly peptides) have been found in addition to CHCs both on the cuticle and on the comb surface of social insects, and their semiochemical role has been demonstrated in some circumstances. In the present study, we used the paper wasp social parasite-host system Polistes sulcifer (Zimmerman)-Polistes dominulus (Christ) to evaluate the relative importance of the CHCs and polar compounds in two different steps of the host exploitation process: host nest detection by the pre-usurping parasite and parasite chemical integration into the host colony. After separating the polar and apolar fractions of the host nest as well as those of pre- and post-usurpation parasites, we carried out laboratory assays based on the binary choice model. Our results show that nest polar compounds neither are used by the parasite to detect the host's nest nor play a role in parasite chemical integration into the host colony. In contrast, we demonstrate that CHCs are fundamental in both steps, thus confirming their primary role in social insect life and consequently in social parasite-host interactions.
Social parasitism describes a fascinating way of life in which species exploit the altruistic behaviour of closely related, social species. Social parasites have repeatedly evolved in the social Hymenoptera, including ants, bees, and wasps. The common ancestry and shared (social) environment with their hosts facilitates the study of molecular adaptations to the parasitic lifestyle. Moreover, when social parasites are widespread and virulent, they exert strong selection pressure on their hosts, leading to the evolution of defense mechanisms and triggering a coevolutionary arms race. Recent advances in sequencing technology now make it possible to study the molecular basis of this coevolutionary process. In addition to describing the latest developments, we highlight open research questions that could be tackled with genomic, transcriptomic, or epigenetic data.
Social recognition, i.e. The ability to recognize and assign individual membership to a particular and relevant class, such as caste, dominance status, gender or colony, shapes the amazing organization of insect societies. Traditionally, it has been assumed that social recognition in social insects is mainly governed by chemicals. However, social insects also share information via many other sensory channels, and it has been recently demonstrated that visual signals can mediate several types of social recognition in some species of social wasps. Primitively social wasps, such as paper wasps of Polistes genus, are suitable models to investigate visual communication because their combs lack of envelops allowing light to produce visual cues, their colonies are small, they have a good vision, they show a remarkable individual within-colony colour variation and, finally, they show an intense social life based on social recognition. In this chapter we reviewed the role of visual cues in social recognition inside and outside social wasp colonies focusing both on the intraspecific and interspecific recognition contexts.
Contrasting phenotypes arise from similar genomes through a combination of losses, gains, co-option and modifications of inherited genomic material. Understanding the molecular basis of this phenotypic diversity is a fundamental challenge in modern evolutionary biology. Comparisons of the genes and their expression patterns underlying traits in closely related species offer an unrivaled opportunity to evaluate the extent to which genomic material is reorganized to produce novel traits. Advances in molecular methods now allow us to dissect the molecular machinery underlying phenotypic diversity in almost any organism, from single-celled entities to the most complex vertebrates. Here we discuss how comparisons of social parasites and their free-living hosts may provide unique insights into the molecular basis of phenotypic evolution. Social parasites evolve from a eusocial ancestor and are specialized to exploit the socially acquired resources of their closely-related eusocial host. Molecular comparisons of such species pairs can reveal how genomic material is re-organized in the loss of ancestral traits (i.e., of free-living traits in the parasites) and the gain of new ones (i.e., specialist traits required for a parasitic lifestyle). We define hypotheses on the molecular basis of phenotypes in the evolution of social parasitism and discuss their wider application in our understanding of the molecular basis of phenotypic diversity within the theoretical framework of phenotypic plasticity and shifting reaction norms. Currently there are no data available to test these hypotheses, and so we also provide some proof of concept data using the paper wasp social parasite/host system (Polistes sulcifer—Polistes dominula). This conceptual framework and first empirical data provide a spring-board for directing future genomic analyses on exploiting social parasites as a route to understanding the evolution of phenotypic specialization.
1. Like avian brood parasites, obligate insect social parasites exploit the parental care of a host species to rear their brood, causing an evident loss of host reproductive success. This fitness cost imposes selective pressure on the host to reduce the parasite effect. A possible outcome of an evolutionary arms race is the selection of host morphological counter-adaptations to resist parasite attacks.
2. We studied host–parasite pairs of Polistes wasps in which the fighting equipment of the parasite's body allows it to enter the host colony.
3. We searched for host morphological traits related to fighting ability that could be considered counter-adaptations. As a host–parasite co-evolutionary arms race can only occur where the two lineages co-exist, we compared morphological traits of hosts belonging to populations with or without parasite pressure. We report that host foundresses belonging to populations under strong parasite pressure have a larger body size than those belonging to populations without parasite pressure.
4. Behavioural experiments carried out to test if an increase in host body size is useful to oppose parasite usurpation show that large body size foundresses exhibit a greater ability of nest defence.
Greenberg's landmark publication (Science 206[1979]: 1095-1097) on kin recognition in sweat bees was followed closely by experimental studies of kin recognition in primitively eusocial paper wasps. These early studies of recognition in social wasps concentrated on documenting nestmate recognition ability, which then stimulated interest in the mechanism subserving recognition ability. For the major portion of my review, I summarize our current understanding of kin, brood, and nest recognition ability in social wasps and its underlying mechanism, relying primarily on paper wasps (Polistes) as a model system. In my discussion of the mechanism of recognition, I review our understanding of the perception, expression, and action components of recognition. I also provide a synopsis of the recent recognition studies of two species of Polistes and their congeneric, obligate social parasites. Finally, I discuss our understanding of the ecology of kin recognition in social wasps and then close my review by contemplating the future directions of kin recognition research.
A social parasite uses workers of another social insect species to rear its own progeny. They are often so closely related to their hosts that it has been suggested that they could have evolved sympatrically from them. To address the question of whether social parasites evolved from their hosts we present a partial sequence of the mitochondrial 16S rRNA gene for nine species of Polistes, comprising all known species of social parasites, their hosts and two outgroups. Parsimony and maximum-likelihood analyses of the data support monophyly for these social parasites. The trees supporting monophyly are significantly shorter than the trees supporting sympatric speciation of parasites from their hosts. These data support the hypothesis that speciation occurred allopatrically and independently of the evolution of social parasitism. Where the social parasite parasitizes more than one species, the two species used are most closely related to each other. Although social parasites are monophyletic and did not evolve sympatrically from their hosts, it is clear that relatedness among species is important in the host-parasite relation.
The cycle of colonies of Polistes biglumis bimaculatus invaded by the obligate and permanent social parasite Polistes atrimandibularis differs from that of normal colonies of the same species as an effect of the presence of the inquiline. In parasitized nests the host foundresses disappear sooner than they do from non parasitized ones and P. b. bimaculatus emergences are both limited in time and reduced in number. After a brief temporal gap from the end of the host emergence period parasite offspring begin to appear in invaded colonies and continue to emerge until the end of the season. In parasitized colonies the number of P. b. bimaculatus emergences is reduced by half with respect to non‐parasitized colonies, while the total number of emerged individuals (host plus parasite brood) is greater than that observed in normal colonies (only P. b. bimaculatus brood). Changes in colony cycle and loss in host brood production in parasitized nests are discussed.
Lorenzi, M. C. 2006: The result of an arms race: the chemical strategies of Polistes social para-sites. — Ann. Zool. Fennici 43: 550–563. The ability of social insects to discriminate between nestmates and aliens on the basis of scent has been the selective pressure favoring the evolution of chemical strategies to facilitate integration into host nests by social parasites, i.e., by organisms which rely on the nests and workers of others to rear their brood. As a result of the coevolu-tionary arms race, obligate social parasites of Polistes wasps have evolved complex mechanisms of mimicry. Social parasites mimic host chemical signatures at the level of species, colony, and possibly rank. Social parasites possess diluted recognition cues and apply compounds to the host nests that may result in host manipulation. The origin and evolutionary pathway to host/parasite chemical similarity is discussed by making comparisons with the tactics used by facultative social parasites, and with the develop-ment of the cuticular signature in free-living species.
High-resolution genetic markers have revolutionized our understanding of vertebrate mating systems, but have so far yielded few comparable surprises about kinship in social insects. Here we use microsatellite markers to reveal an unexpected and unique social system in what is probably the best-studied social wasp, Polistes dominulus. Social insect colonies are nearly always composed of close relatives; therefore, non-reproductive helping behaviour can be favoured by kin selection, because the helpers aid reproductives who share their genes. In P. dominulus, however, 35% of foundress nestmates are unrelated and gain no such advantage. The P. dominulus system is unlike all other cases of unrelated social insects, because one individual has nearly complete reproductive dominance over subordinates who could have chosen other reproductive options. The only significant advantage that subordinates obtain is a chance at later reproduction, particularly if the queen dies. Thus, P. dominulus societies are functionally unlike other social insects, but similar to certain vertebrate societies, in which the unrelated helpers gain through inheritance of a territory or a mate.
In this synthesis we apply coevolutionary models to the interactions between socially parasitic ants and their hosts. Obligate social parasite systems are ideal models for coevolution, because the close phylogenetic relationship between these parasites and their hosts results in similar evolutionary potentials, thus making mutual adaptations in a stepwise fashion especially likely to occur. The evolutionary dynamics of host-parasite interactions are influenced by a number of parameters, for example the parasite's transmission mode and rate, the genetic structure of host and parasite populations, the antagonists' migration rates, and the degree of mutual specialisation. For the three types of obligate ant social parasites, queen-tolerant and queen-intolerant inquilines and slavemakers, several of these parameters, and thus the evolutionary trajectory, are likely to differ. Because of the fundamental differences in lifestyle between these social parasite systems, coevolution should further select for different traits in the parasites and their hosts. Queen-tolerant inquilines are true parasites that exert a low selection pressure on their host, because of their rarity and the fact that they do not conduct slave raids to replenish their labour force. Due to their high degree of specialisation and the potential for vertical transmission, coevolutionary theory would predict interactions between these workerless parasites and their hosts to become even more benign over time. Queen-intolerant inquilines that kill the host queen during colony take-over are best described as parasitoids, and their reproductive success is limited by the existing worker force of the invaded host nest. These parasites should therefore evolve strategies to best exploit this fixed resource. Slavemaking ants, by contrast, act as parasites only during colony foundation, while their frequent slave raids follow a predator prey dynamic. They often exploit a number of host species at a given site, and theory predicts that their associations are best described in terms of a highly antagonistic coevolutionary arms race.
The diversity of social behavior among birds and primates is surpassed only by members of the Hymenopteran insects, including bees, ants, and the genus Polistes, or paper-wasps. This volume combines incisive reviews and new, unpublished data in studies of paper-wasps, a large and varied group whose life patterns are often studied by biologists interested in social evolution. While this research is significant to the natural history of paper-wasps, it also applies to topics of general interest such as the evolution of cooperation, social parasitism, kin recognition, and the division of labor.
This book is the first to present a comprehensive overview of parasitic birds and their hosts. Although the phenomenon has attracted the interest of naturalists and evolutionists since Darwin, only recently have researchers applied modern evolutionary theory and experimental methods to study the various adaptations related to brood parasitism. The work in this field is accelerating rapidly, and this volume collects work from the individuals and research groups around the world who have been responsible for nearly every major study in the last ten years. The papers present valuable summaries along with substantial new research, and the volume concludes with a review of important unsolved questions. The book is an invaluable resource on this fascinating topic, covering the remarkable sequences of adaptations and counter-adaptations, along with the perhaps even more remarkable cases where adaptations seem to be lacking.
The results of a morphological and morphometric comparison between two species of Polistes obligate social parasites and their two respective host species are reported. Some parts of the body of the parasites were found to be larger than those of their hosts. Probably, such morphological traits are an advantage to the parasites during the nest invasion fights, e.g. the size of the mandibles which they use as a weapon against the foundress and workers. The lack of morphological modifications due to the reduction or loss of some activities and/or behaviours suggest that Polistes social parasites should not be considered as having attained a high degree of parasitic specialization.
The population structure of the mycophagous beetle P. substriatus is characterized by many small local populations interconnected by migration over a small spatial scale (10×75 m2). Each local P. substriatus population has a relatively short expected persistence time, but persistence of the species occurs due to a balance between frequent local extinctions and recolonizations. This non-equilibrium population structure can have profound effects on how the genetic variation is structured between and within populations. Theoretical models have stated that the genetic differentiation among local populations will be enhanced relative to an island model at equilibrium if the number of colonizers is less than approximately twice the number of migrants among local populations. To study these effects, a set of 50 local P. substriatus populations were surveyed over a four year period to record any naturally occurring extinctions and recolonizations. The per population colonization and extinction rate were 0.237 and 0275, respectively. Mark-recapture techniques were used to estimate a number of demographic parameters: local population size (N=11.1), migration rate (=0.366), number of colonizers (k=4.0) and the probability of common origin of colonizers (φ=0.5). The theoretically predicted level of differentiation among local populations (measured as Wright’s FST) was 0.070. Genetic data obtained from an electrophoretic survey of 7 polymorphic loci gave an estimated degree of differentiation of 0.077. There was thus a good agreement between the empirical results and the theoretical predictions. Young populations (young=0.090) had significantly higher levels of differentiation than old, more established populations (old=0.059). The extinction-recolonization dynamics resulted in an overall increased in the genetic differentiation among local populations by c. 40%. The overall effective population size was also reduced by c. 35%. The results give clear evidence to how non-equilibrium processes shape the genetic structure of populations.
Studies on avian cuckoos have demonstrated that parasite chicks compete with host fledglings to monopolize food or manipulate the foster parents to increase their provisioning rate. This topic has never been explicitly investigated in insect social parasites, which use the social system of another species to raise their brood. Here we show that the immature brood of the cuckoo wasp Polistes sulcifer grows more rapidly than the host immature brood. Host workers perform more parental care to parasite larvae than to conspecific ones. Thus, the rapid growth of the parasite larvae is evidently due to increased host care, which prolongs the development of host larvae reared in the same colony. We suggest that parasite larvae play an active role in host exploitation through manipulation of host workers, as occurs in parasitic birds.
Polistes sulcifer is a cuckoo paper wasps, an obligate social parasite which must usurp a colony of another species in order to reproduce. Field data show thatP. sulcifer females usurp exclusively nests belonging to one species only (P. dominulus). Moreover, they are more frequently found on large and puparich nests. A series of laboratory trials, in which parasite females were offered a binary choice of nests with different characteristics, confirm both the species specificity betweenP. sulcifer andP. dominulus and the parasite's preference to usurp larger nests containing pupae. The data support the hypothesis thatP. sulcifer females choose between available nests. The biological meaning of these findings is discussed.
The main characteristics of invasion of a Polistes dominulus Christ colony by a female of Sulcopolistes sulcifer Zimmermann can be summarized as follows: the parasite is usually attacked by Polistes while still approaching the nest. The parasite fights all opponents on the ground, both foundresses and workers, some of which can be very aggressive even off the nest. Others succumb to the parasite immediately on the very first encounter. Sulcopolistes' strategy is to fight one adversary at a time and then return rapidly to the nest. In this way it is easier for her to defeat the hosts one after another, and to usurp nests with a high number of workers. While fighting on the ground the parasite never used its sting, but tried to bite the legs off its victims. The alpha foundress is the one which attacks the parasite most aggressively, which in turn is particularly aggressive towards her. Beta females on bigynic and gamma females on trigynic foundations are less aggressive than their nestmates of higher hierarchical status. After nest conquest, dominance activity of the parasite increases, and she offers drops of liquid to nest occupants during encounters. When not interacting with the hosts, Sulcopolistes performs an intense nest inspection and carefully strokes the nest surface and internal parts of some cells with her abdominal sterna.
Cervo, R. 2006: Polistes wasps and their social parasites: an overview. — Ann. Zool. Fennici 43: 531–549. Severe brood care costs have favoured the evolution of cheaters that exploit the paren-tal services of conspecifics or even heterospecifics in both birds and social insects. In Polistes paper wasps, three species have lost worker castes and are dependent on hosts to produce their sexuals, while other species use hosts facultatively as an alternative to caring for their own brood. This paper offers an overview of the adaptations, strategies and tricks used by Polistes social parasites to successfully enter and exploit host social systems. Moreover, it also focuses on the analogous solutions adopted by the well-known brood parasite birds, and stresses the evolutionary convergence between these two phy-logenetically distant taxa. A comparative analysis of life-history patterns, as well as of phylogenetic relationships of living facultative and obligate parasitic species in Polistes wasps, has suggested a historical framework for the evolution of social parasitism in this group. As with avian brood parasites, the analysis of adaptation and counter adaptation dynamics should direct the future approach for the study of social parasitism in Polistes wasps. The Polistes parasite–host system seems a suitable candidate for a model system in coevolutionary arms race studies, just as Polistes paper wasps have been considered for many years a model organism for sociobiological studies.
Summary. We report that the social parasite Polistes atrimandibularis (Zimmermann) can exploit at least three more host species than previously described. One of these, P. associus, has never been reported as host of a social parasite. Our data show no constraints in host choice, indicating P. atrimandibularis is a generalist social parasite.
Summary: Polistes dominulus, a common Polistes species with Old World distribution, is now invading the United States. We discuss those characteristics of P. dominulus that may explain its successful establishment in its new American environment. A versatile diet, the ability to colonize new environments and a short development time of the immature brood might have played an important role in the rapid spread in P. dominulus.
Coevolution is one of the major processes organizing the earth's biodiversity. The need to understand coevolution as an ongoing process has grown as ecological concerns have risen over the dynamics of rapidly changing biological communities, the conservation of genetic diversity, and the population biology of diseases. The biggest current challenge is to understand how coevolution operates across broad geographic landscapes, linking local ecological processes with phylogeographic patterns. The geographic mosaic theory of coevolution provides a framework for asking how coevolution continually reshapes interactions across different spatial and temporal scales. It produces specific hypotheses on how geographically structured coevolution differs from coevolution at the local scale. It also provides a framework for understanding how local maladaptation can result from coevolution and why coevolved interactions may rarely produce long lists of coevolved traits that become fixed within species. Long-term field studies of the same interaction across multiple communities and spatially structured mathematical models are together beginning to show that coevolution may be a more important ongoing process than had been indicated by earlier empirical and theoretical studies lacking a geographic perspective.
Traditional ecological approaches to species evolution have frequently studied too few species, relatively small areas, and relatively short time spans. In The Coevolutionary Process, John N. Thompson advances a new conceptual approach to the evolution of species interactionsâthe geographic mosaic theory of coevolution. Thompson demonstrates how an integrated study of life histories, genetics, and the geographic structure of populations yields a broader understanding of coevolution, or the development of reciprocal adaptations and specializations in interdependent species. Using examples of species interactions from an enormous range of taxa, Thompson examines how and when extreme specialization evolves in interdependent species and how geographic differences in specialization, adaptation, and the outcomes of interactions shape coevolution. Through the geographic mosaic theory, Thompson bridges the gap between the study of specialization and coevolution in local communities and the study of broader patterns seen in comparisons of the phylogenies of interacting species.
An adaptation in one lineage (e.g. predators) may change the selection pressure on another lineage (e.g. prey), giving rise to a counter-adaptation. If this occurs reciprocally, an unstable runaway escalation or 'arms race' may result. We discuss various factors which might give one side an advantage in an arms race. For example, a lineage under strong selection may out-evolve a weakly selected one (' the life-dinner principle'). We then classify arms races in two independent ways. They may be symmetric or asymmetric, and they may be interspecific or intraspecific. Our example of an asymmetric interspecific arms race is that between brood parasites and their hosts. The arms race concept may help to reduce the mystery of why cuckoo hosts are so good at detecting cuckoo eggs, but so bad at detecting cuckoo nestlings. The evolutionary contest between queen and worker ants over relative parental investment is a good example of an intraspecific asymmetric arms race. Such cases raise special problems because the participants share the same gene pool. Interspecific symmetric arms races are unlikely to be important, because competitors tend to diverge rather than escalate competitive adaptations. Intraspecific symmetric arms races, exemplified by adaptations for male-male competition, may underlie Cope's Rule and even the extinction of lineages. Finally we consider ways in which arms races can end. One lineage may drive the other to extinction; one may reach an optimum, thereby preventing the other from doing so; a particularly interesting possibility, exemplified by flower-bee coevolution, is that both sides may reach a mutual local optimum; lastly, arms races may have no stable and but may cycle continuously. We do not wish necessarily to suggest that all, or even most, evolutionary change results from arms races, but we do suggest that the arms race concept may help to resolve three long-standing questions in evolutionary theory.
In multiple-foundress nests of the wasp Polistes dominulus, dominance hierarchies are established among foundresses, and only the dominant (=alpha) individual lays eggs. The alpha female can be distinguished from subordinate females and workers on the basis of the proportions of some hydrocarbons present on the cuticle, suggesting that chemical signaling of her reproductive status could occur. P. dominulus is also the host species of the obligate social parasite Polistes sulcifer. After aggressively usurping host colonies and behaviorally replacing the host alpha female, parasites are characterized by a change in the proportions of their cuticular hydrocarbons to match that of the host cuticular profile at both species and colony levels. In the current study, we demonstrate that P. sulcifer queens also modify their cuticular hydrocarbon proportions after usurpation to match that of the host alpha female. Parasite females, therefore, acquire the dominant rank in host colonies both reproductively and chemically by mimicking the typical alpha profile of the host. Parasite females were not able to fully inhibit ovary development in host foundresses, and 10 days after usurpation, parasites, alpha and beta foundresses show similar chemical profiles and ovarian development.
Infanticide in colonies of social wasps Pro-tection and abuse of young in animals and man
- S Turillazzi
- R Cervo
Turillazzi S, Cervo R. 1994. Infanticide in colonies of social wasps. In: Parmigiani S, Square B, Von Saal F, eds. Pro-tection and abuse of young in animals and man. New York, NY: Harwood Academic.
Foraging activity in European Polistes wasps (Hymenoptera, Vespidae)
- A Nannoni
- R Cervo
- Turillazzi
Nannoni A, Cervo R, Turillazzi S. 2001. Foraging activity in European Polistes wasps (Hymenoptera, Vespidae). Bollettino Società Entomologica Italiana 133: 67–78.
Overview and commen-tary
- Rothstein Si
- Robinson
- Sk
Rothstein SI, Robinson SK. 1998. Overview and commen-tary. In: Rothstein SI, Robinson SK, eds. Parasitic birds and their hosts. Oxford: Oxford University Press, 3–38.
Il parassitismo sociale nei Polistes
- R Cervo
Foraging activity in European Polistes wasps (Hymenoptera, Vespidae)
- Nannoni