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A model for the evolution of parasite-host interactions based on the Maculinea-Myrmica system: Numerical simulations and multiple host behavior
Abstract
We present a mathematical model of parasite–host interactions inspired by the Maculinea–Myrmica system. Numerical simulations of the model were conducted in order to access the possibility of stable multiple host behavior in the model. Results indicate that multiple host behavior can be observed under natural conditions, although a division of the original parasite population into separate subpopulations, each adapted to one distinct host, is expected. Transitions from single to multiple host behavior are expected to occur if the relative host species abundances change or host’s tolerance increases. Further model development and analysis are required to extend these results.
... In the model proposed in this paper, host specificity is allowed to vary. Assis et al. (2012) have developed a model for the evolution of host specificity patterns, using a simplification of the population dynamics and considering a "phenotype space" (or an "aspect space"), where the populations could evolve. The model indicates that multiple host behaviour could evolve and be stable, with the parasite population splitting in two subpopulations, each adapted to one host. ...
... The purpose of this paper is to extend the results of Assis et al. (2012) by suitably accounting for interspecific competition between Myrmica species, although using a somewhat simplified mathematical system. The role and usefulness of mathematical models lies in the possibility of performing simulations when real data are lacking or insufficient, to infer information about the possible system's behaviour. ...
... Each point denotes an observation site closer to its primary host than other non-host Myrmica species (Akino et al. 1999;Schönrogge et al. 2004;Schlick-Steiner et al. 2004;Nash et al. 2008;Thomas et al. 2013). Based on such evidence, Assis et al. (2012) developed a model that considers the populations of parasites and potential hosts evolving in a phenotypic space. The findings suggested that multiple host behaviour could be observed in the Maculinea-Myrmica system, with the parasite population splitting into two subpopulations, each adapted to one host. ...
A model of interspecific host competition in a system with one parasite (butterfly—Maculinea) and multiple potential hosts (ants—Myrmica) is presented. Results indicate that host interspecific competition increases the occurrence of multiple host behaviour in Maculinea natural populations but decreases the ability of the parasite populations to adapt to the most abundant host species. These qualitative predictions were compared with data on host specificity, with good agreement. Analysis of the data also indicates that Maculinea teleius and Maculinea arion respond differently to changes in relative host abundances. Maculinea teleius shows a larger fraction of sites where it displays multiple host behaviour and a larger fraction of sites where the niches of the hosts overlap. In some instances, Maculinea teleius is adapted to Myrmica hosts that are present in lower frequencies. Maculinea arion is locally more host-specific and occurs at sites where host interspecific competition is unlikely and is more frequently adapted to the most abundant host species.
... Evolutionary theory and observations suggests that host-parasite systems can display a great diversity of behaviors: (i) unending arms-race between host and parasite (Soler et al., 2001;Langmore and Kilner, 2010), (ii) stalemates (Berenbaum and Zangerl, 1988), (iii) extinction of one or both species (Dunn et al. 2009) and (iv) "victory" by the parasite (Als et al. 2004;Langmore and Kilner, 2010). This variety of behaviors indicates that the outcomes of a particular system will depend on particularities of the host-parasite system and could be influenced even at a local scale by the ecological context (Abrams and Matsuda, 1997;Assis et al., 2012). ...
... For the modelling process we adopt an aspect-space approach derived from classical models in mathematical biology (Segel, 1988;Murray, 1989). This approach has been used in the study of biological systems (Lin et al., 2003;Assis et al., 2012;Ferreira Jr. and Marcon, 2014) and can present an alternative way to model evolutionary dynamics (Assis and Ferreira Jr., 2016), frequently described by models of Population Genetics (Taylor and Higgs, 2000), Game Theory (Smith, 1982;Weibull, 1997) or other approaches (Nowak 2006). ...
... Once the relations between traits and a set Ω are well-established, the three fundamental mechanisms of evolution can be described using the following dynamics for the aspect-space distribution , (Assis, 2012;Assis et al., 2012;Assis and Ferreira Jr., 2016): ...
We present a theory for the evolution of multiple host use in the parasite-host system Maculinea-Myrmica. A mathematical model supporting the theory is presented and some results from simulations discussed. Qualitative predictions from simulations of the model are tested using empirical data on the chemical profiles of population of hosts and parasites. The results show that increased similarity between the profiles of the host species is correlated with multiple host use, as predicted by the model. The model provides a theoretical framework which is totally coherent with: (1) patterns of host use by the Maculinea cuckoo species and (2) phylogenetic studies that suggest host shift during the evolutionary history of the species. The results also suggest that it might be possible to create a method to infer host use by the parasite species, based only on cuticular hydrocarbon profiles. Such method would be important for conservation measures.
... To model selection through differential mortality rates, we are going to use an aspect-space approach [2]. Such approach has been used, for example, to model the evolution of host-specificity behaviour in host-parasite systems [1] and shows theoretical consistency with other approaches [2]. It consists, basically, of describing a population as distributed in an aspect space (or trait space) and writing the dynamics that contain the three fundamental conditions for evolution to occur [20,21]. ...
... It consists, basically, of describing a population as distributed in an aspect space (or trait space) and writing the dynamics that contain the three fundamental conditions for evolution to occur [20,21]. For the details on the construction of models using this approach we refer to [1,2]. ...
In this work, a partial differential equation model for evolutionary dynamics is presented that describes changes in densities of phenotypes in a population. We consider that the traits of individuals of a population are distributed at an interval of real numbers where a mortality rate is assigned for each value of this interval. We present some conditions for stability of stationary solutions and apply the model in theoretical scenarios of natural selection. Particularly we approach cases of stabilising, disruptive and directional selection, including the scenario of the survival of the flattest. Some computational simulations are performed to illustrate the results obtained.
... The fact that we do not observe multiple-host use, i.e. transient populations, often, suggests transitions are quick. A mathematical model based on the Phengaris system also suggests that multiple-host use can arise in both a transient or stable state, while single host use is the more likely outcome across a wide range of the parameter space 43 . A separate modelling approach also suggested that multiple-host use is more likely on sites where the similarity between the chemical profiles of distinct host ant species is high. ...
In natural ecosystems, relationships between organisms are often characterised by high levels of complexity, where vulnerabilities in multi-trophic systems are difficult to identify, yet variation in specific community modules can be traceable. Within the complex community interactions, we can shed new light on dynamics by which co-evolutionary outcomes can inform science-led conservation. Here we assessed host-ant use in six populations of the butterfly Phengaris (=Maculinea) rebeli, an obligate social parasite of Myrmica ants and a model system in evolutionary and conservation ecology. Starting from the initial distribution of eggs, we estimated the survival of the parasite in the wild in nests of seven Myrmica ant species, and analysed the chemical cues evolved by the parasites to subvert its host defences. We found local variations in host specificity that are consistent with similarities found in the chemical profiles of hosts and parasites on different sites. At some sites, only one ant species is successfully exploited; at others, multiple-host populations are used. Understanding how stable or adaptable these associations are is essential knowledge when devising conservation measures to maintain keystone species of ant and locally adapted populations of Phengaris butterfly species, which are rare, threatened and a high priority for conservation worldwide.
... 2. Creation of specific models: developing models for specific biological examples is a great way to test if this type of model can produce interesting results from the biological point of view. Assis et al. (2012) have developed a model for host-parasite interaction in the case of the Maculinea-Myrmica system and, although the results are consistent with biological observations, those could not be subject to quantitative testing because of its qualitative characteristics. The creation of further models could establish more clearly the advantages of this kind of approach. ...
We present a reaction–diffusion mathematical model for the evolutionary dynamics of phenotypic evolution. A detailed deduction of the equations is presented for the one-dimensional version, from which a more general model is proposed. Particular cases are studied using analytical approximations and numerical simulations. Results indicate that the approach proposed produces results that are coherent with mainstream models in evolutionary dynamics, suggesting that the reaction–diffusion model could be an alternative tool in the analysis of evolutionary dynamics.
... Parameters: a = 0.9, b = 0.05, a 1 = 0.6, a 2 = 0.4, a 3 = 0.3, a 4 = 0.5, a 5 = 0.7 (r = a + 1), e = 0.01, N 0 = 0.3. the more toxic species would eventually become subjected to a higher predation rate from unlearned predators (resulted from their occasional testing of more palatable and mimicking species) it is conceivable that an escape from the common pattern is advantageous to the more toxic species, while the lesser toxic species would keep ''following'' their mutation footsteps (Sherratt, 2008;Assis et al., 2012). As Mü ller already pointed out in his 1879 paper, although Mü llerian Mimicry is a ''cooperative'' process where both species profit from their convergence in pattern space, even though the smaller population gets more reproductive advantage than the more numerous species. ...
In this paper we present some novel mathematical approaches to describe an extraordinary phenomenon widely cited in the biological literature as “Müllerian Mimicry”. Mimicry in general is an evolutionary phenomenon which was observed and registered in the scientific literature a long time ago by Henry W. Bates in a form named “Batesian” today. Müllerian Mimicry is a subtle phenomenon from an evolutionary point of view and happens when two different species, both of them toxic as well, and under pressure from the same predator, develop a similar strong visual signal in such a way that “teaching casualties” become a shared onus. The tasting of any individual, no matter from which prey population, will turn the hapless predator into a “learned” one which will treat both prey populations with due respect afterwards. This type of Mimicry among butterflies having birds as their main predators was first described by Fritz Müller, a German-Brazilian naturalist in a paper published in 1879 which emphasized the learning dynamics of predators. Besides the formulation of the main principles for studying such phenomenon, Müller argued his ideas with one of the first mathematical model of evolutionary theory. In this paper we present some of Müller's ideas in a framework general enough to be represented by mathematical models. As an example we formulate a conceptual simple discrete-time model and discuss a number of simulations which exemplify many observable aspects of Müllerian Mimicry.
In our discussion we will always keep in mind the real examples represented by butterflies as prey populations and birds as their predators which in fact were the case originally studied by Müller and still is one of the more important instances where Mimicry phenomena occur in nature. However, we try to expound a sufficiently general scheme that could support many mathematically specific models for predator learning dynamics and signaling communication.
Résumé
L'azuré des moulières (Maculinea alcon) est un papillon myrmécophile stricte. Ce qui veut dire que la conservation de ce papillon implique la conservation des espèces de fourmis qui sont les nourrices de ses chenilles (Myrmica spp.). Dans la Vienne ce lépidoptère protégé est étudié dans l'unique station régionale où l'espèce est encore présente : le Pinail. Au total, 229 pièges à fourmis ont été disposés sur des transects sur trois secteurs de gestion (fauche, brulis, pâturage). Les modes de gestion ont permis de comparer la richesse spécifique en fourmis et plus particulièrement en espèce susceptible d'élever les chenilles de Maculinea alcon (c.-à-d.: Myrmica scabrinodis, M. ruginodis, M. schenkii). Les inventaires indiquent une plus forte diversité dans le pâturage par rapport aux milieux oligotrophes que sont les zones de fauche et de brulis. Les zones avec plus forte abondance de gentianes ont moins d'espèces de fourmis nourrices, et les fleurs ont moins de pontes. Les résultats suggèrent une pression de parasitisme négative sur les fourmis nourrices et une potentielle capacité des paillons de reconnaitre des zones favorables de pontes (=fleur+nourrice <2m). Les mesures de conservation proposées sont le maintien de mosaïques d'habitats favorables différentiellement aux gentianes (fauché, brulé) et d'autres zones favorables aux Myrmica nourrices (paturé, lande agée/fermé) pour garantir des milieux sources de fourmis et in fine favoriser la population de Maculinea alcon.
Abstract
The alcon blue (Maculinea alcon) is a strict myrmecophile butterfly. This means that the conservation of the butterfly involves the conservation of ant species (Myrmica spp.) which are the nurses of its caterpillar. In the Vienne French department this protected rhopalocera is studied in the last remaining regional station: the Pinail. 229 ant traps were placed on transects in three different management areas (mowing, burning, grazing). The management methods were used to compare ant species richness and especially in nurse species likely to raise the Maculinea caterpillars (ie: Myrmica scabrinodis, M. ruginodis, M. schenkii). Inventories indicate greater diversity in the pasture compared to oligotrophic areas (mowing, burned). Areas with highest abundance of Gentiana flowers have fewer species of ant nurses, and the flowers have fewer clutches. The results suggest a negative parasitism pressure on nurses ants and a potential capacity of the butterfly to recognize favorable areas of spawning (= flower+nurse <2m). The proposed conservation measures are to maintain a mosaic of habitats: favorable for gentians (mowed, burned) and other areas favorable to Myrmica nurses (pasture, old moorland) in order to secure ant sources for surrounding environment and ultimately promote the population of Maculinea alcon.
A mathematical model of the interaction between two levels of selection (intracellular and cellular) is presented. The paradigm is that of a selfish intracellular replicator, such as a strand of selfish DNA, that reproduces itself at the expense of the efficiency of the structure of the cell. A mathematical analysis is conducted and conditions for the survival of the selfish replicators are obtained explicitly. Our results indicate that, if reproduction is asexual, mechanisms of horizontal transfer of genes are essential for the fixation of such replicators in the population and also that less harmful replicators have a better chance of infecting a whole population, while aggressive ones will usually successfully infect only a part of it.
Abstract
Although most conservationists claim to protect “species”, the conservation unit actually and practically managed is the
individual population. As resources are not unlimited, we need to focus on a restricted number of populations. But how can
we select them? The Evolutionarily Significant Unit (ESU), first conceptualised by Ryder in 1986, may offer some answer.
Several definitions have been proposed for the ESU, but all make reference to units “whose divergence can be measured or
evaluated by putting differential emphasis on the role of evolutionary forces at varied temporal scales”. Thus, an ESU might
be fully identical with a “species”, or a “species” could be composed of multiple ESUs. On the other hand, an ESU might
comprise single/multiple populations exchanging a degree of gene flow, such as meta-populations. In an attempt to show
strengths and weaknesses of ESU concepts, we present here, among several others, some case studies on the myrmecophilous
butterflies of the genus Maculinea. In particular, we analyse the apparently everlasting debate about Maculinea alcon and
M. rebeli, whose separation into separate species has been accepted by many authors, on mainly ecological criteria, but has
not been fully supported by molecular analyses. We also discuss how the tight association with host ants may have driven
selection for increasingly more strictly adapted Maculinea populations, arguably deserving specific taxonomic identity.
Finally we discuss how current DNA analyses may fail to detect critical information on differences between taxa recently
originated by the action of separate adaptive processes, which non-molecular studies can sometimes reveal. We conclude by
discussing some current and often conflicting taxonomic trends, in their relationships with conservation policies.
We study the dynamics of a one-predator, two-prey system in which the predator has an indirect effect on the preys. We show that, in presence of the indirect effect term, the system admits coexistence of the three populations while, if we disregard it, at least one of the populations goes to extinction.
Maculinea teleius Bgstr. and M. nausithous Bgstr. larvae are obligatory social parasites of Myrmica Latr. ants spending most of their immature life inside ant nests and praying on ant brood. Studies were made to determine host-ant specificity of M. teleius and M. nausithous in Poland. Research was performed on: two isolated sites of M. teleius, one isolated site of M. nausithous and one site where populations of both species occurred as a part of the metapopulation system. Our findings showed that M. nausithous is the more specialized species living exclusively in nests of M. rubra L. while M. teleius seemed to be more plastic and adapted to local ants. Its larvae were recorded in nests of four Myrmica species with the highest frequency in M. rubra colonies. M. gallienii Bondr. was detected for the first time as a host-ant of M. teleius (or any Maculinea van Eecke species). The frequency of M. teleius larvae in M. gallienii nests was similar to that observed in M. scabrinodis Nyl. - the 'classic' host-ant of M. teleius in Europe. Results are discussed with respect to Maculinea biology and conservation.
Butterflies of the genus Phengaris have a highly specialised life cycle involving an obligatory relationship with Myrmica ants. A knowledge of the host ant specificity is essential for understanding the relationship between a particular Phengaris species and its hosts and also important for the conservation of these butterflies. Data on host ant specificity were collected in Poland, the Czech Republic, Slovakia and Ukraine. Five different Myrmica species were used by P. teleius as hosts (M. scabrinodis, M. rubra, M. ruginodis, M. rugulosa and M. gallienii) and at most localities it was not possible to distinguish a primary host - i.e. several Myrmica species were parasitized to similar extents. Three populations of P. nausithous were found in Poland and Ukraine. In every case, M. rubra was its primary host, although in the Krak-acow region (Poland) two nests of M. scabrinodis and two of M. ruginodis were infested by this butterfly species. P. alcon in the four populations investigated in Poland and Ukraine invariably only used M. scabrinodis as a host despite the presence of other Myrmica species. These results obtained suggest lack of host specificity in P. teleius and high host specificity in P. nausithous, which mainly uses M. rubra as its host across Europe. Moreover, the three populations of P. alcon investigated seem to be highly specific and use M. scabrinodis as a host, which confirms the high local specialisation of these populations.
ABStrACt Studies on host-ants of the socially parasitic Large Blue butterfly Phengaris arion were performed at two sites located in different parts of Europe (NW Italy and NE Poland). Both localities differed considerably as far as biotope type was concerned (alpine grasslands vs. road verges in lowland pine forests). We opened and examined 206 colonies of nine Myrmica species in Italy and 146 colonies of seven species in Poland. In the two samples only one and seven nests respectively were infested by the butterfly. The most interesting findings for both localities were single records of M. lonae hosting P. arion, which represents a novelty for this myrmecophilous lycaenid. For the Italian site this is also the first and only observation of a premature of P. arion in an ant colony. M. sabuleti, which had been considered so far as the primary host of the butterfly on xerothermal grasslands, was very rare there. It is therefore excluded that it could support that butterfly population. At the Polish site pupae or larvae of the butterfly were found simultaneously in M. lobicornis, M. schencki and M. sabuleti nests (two nests were infested for each species), which suggests multiple host ant use. Our studies also contribute to basic faunistic knowledge. For M. lonae and M. lobulicornis, found at the Italian site, these are the first records of these ants on a national scale.
We employ an empirically motivated ''case model'' approach to investigate the theoretical foundations for the conservation of the endangered butterfly Maculinea arion. Maculinea butterflies have highly specialized larvae that sequentially exploit a plant and an ant species. Our study establishes that M. arion's specialized life cycle, including scram-ble competition for limiting resources, and the spatially discrete nature of its resources, make it more sensitive to environmental variation and more prone to local extinction than other univoltine phytophagous species. We find that the number and spatial distribution of the butterfly's resources are key factors in their population dynamics, especially for M. arion populations in habitats associated with high larval survival and high adult fecundity. Factors that increase juvenile competition have first a positive effect on adult population size, but beyond a threshold this effect becomes negative. In general, oscillatory dynamics emerge for high potential growth rates and spatially homogeneous juvenile competition. We discuss the relevance of our results to population management, investigate the conse-quences of environmental variation, and consider different scenarios of conservation. Our model, although based on the Maculinea genus, should apply to a broad range of species for which the form of competitive interactions changes predictably at distinct points in the life cycle. Complex life cycles can lead to negative feedbacks involving parameters that are usually thought to optimize population size. We suggest that conservation strategies are neither generalizable for the Maculinea genus nor for disparate populations of each species of Maculinea, and rather that management should be conducted on a case-by-case basis.
Final instar larvae of Maculinea rebeli Hirschke (Lepidoptera, Lycaenidae) are social parasites of Myrmica Latreille (Hymenoptera, Formicidae) nests. In the populations of the southern French Alps and Spanish Pyrenees, >95% adult M. rebeli emerge from colonies of Myrmica schencki Emery, despite >60% caterpillars being adopted by other Myrmica species (non-hosts). However, in laboratory culture caterpillars can be reared successfully by many of the non-host species. This contradiction, which has led some to question the existence of host specificity, has been explained by the lack of stress, particularly food stress, in laboratory cultures compared to wild conditions. Here, we report the results of an experiment that tested the survival of M. rebeli caterpillars that had been growing well, after being socially integrated into a series of host and non-host cultures, and were then subjected to a 4-week period of stress induced by a ‘starvation diet’ estimated to be less than the minimum for ant survival. Significantly more M. rebeli survived in M. schencki cultures than with any of the other Myrmica species (all died in most non-host cultures). Under a starvation diet, caterpillars are killed and eaten along with dead workers – this never happens under an ample diet – rather than simply starving to death. It was noted that the proportion of young M. rebeli caterpillars that survived initial integration into an ant colony (including some M. schencki colonies) was a good predictor of subsequent survival under starvation conditions. We concluded that two key phases of host specificity exist in the life of this social parasite: initial integration, in which the caterpillar simply has to be accepted into a host society, followed by full integration, when a relatively high hierarchical status within the host society becomes essential for a caterpillar's survival during periods when the host colony is stressed, e.g., by food shortage. This experimental regime provides a useful bioassay for testing host specificity in other populations of Maculinea.
1. Phengaris butterflies are obligatory social parasites of Myrmica ants. Early research suggested that there is a different Myrmica host species for each of the five European Phengaris social parasites, but more recent studies have shown that this was an oversimplification.
2. The pattern of host ant specificity within a Phengaris teleius metapopulation from southern Poland is reported. A combination of studying the frequency distribution of Phengaris occurrence and morphometrics on adult butterflies were used to test whether use of different host species is reflected in larval development.
3. Phengaris teleius larvae were found to survive in colonies of four Myrmica species: M. scabrinodis, M. rubra, M. ruginodis, and M. rugulosa. Myrmica scabrinodis was the most abundant species under the host plant but the percentage of infested nests was similar to other host ant species at two sites and lower in comparison to nests of M. rubra and M. ruginodis at the other two sites. Morphometric measurements of adult butterflies reared by wild colonies of M. scabrinodis and M. ruginodis showed that wing size and number of wing spots were slightly greater for adults eclosing from nests of M. ruginodis.
4. Our results suggest that P. teleius in the populations studied is less specialised than previously suggested. The results are consistent with the hypothesis that P. teleius is expected to be the least specific of the European Phengaris species, as it has the largest and best defended fourth-instar caterpillars and, as a predatory species, it spends less time in the central larval chambers of the host colonies. The fact that individuals reared by M. ruginodis had wider hind wings may suggest that P. teleius had better access to resources in M. ruginodis than in M. scabrinodis colonies.
A spatial computer simulation model has been developed to assist our understanding of the ways in which Maculinea butterflies depend upon the spatial distribution and abundance of their initial foodplant and their Myrmica host ant. It was initially derived for the Maculinea rebeli-Myrmica schencki-Gentiana cruciata system. It relates the population processes of the competing host and other ant species to an underlying gradient of habitat quality and incorporates the impact of adopted Maculinea caterpillars on the growth and survival of individual ant nests. The model was initially calibrated for a large site in the Spanish Pyrenees, but has since been successfully tested on 12 French sites and another in Spain. On such sites, with M. rebeli present, there is a close relationship between Maculinea population density and the density of the early larval foodplant G. cruciata. Optimum gentian density is estimated to be about 1500 plants ha-1 on sites with the natural clumping of gentians found. However, any site management which added extra gentians, especially if filling the gaps, is predicted to reduce the Maculinea population. Meta-population studies of single species have shown that the size and spatial arrangement of patches of assumed uniformly suitable habitat can influence their population dynamics and persistence. Our modelling suggests that the spatial pattern of suitable habitat of varied quality within a single site can influence the local butterfly population size and perhaps also persistence. Despite being free-ranging over the whole area, the butterfly''s dynamics may depend on the arrangement of habitat quality at a finer spatial scale, due to its interactions with ant species possessing narrower habitat niches and more localized dispersal. Rapid Science Ltd. 1998
Larvae of Maculinea rebeli, one of the most endangered European butterflies, are obligatory social parasites of Myrmica ants. At present, this relationship is thought to be highly specific, with Myrmica schencki being regarded as the primary host. Here we present data on six populations from Poland and Austria, including the first record of Myrmica specioides as a host, together with published data from other central European countries, which severely questions the inference that M. schencki is the exclusive host of M. rebeli. Our results indicate that Myrmica sabuleti is the most frequently used host ant in central Europe, whereas M. scabrinodis, M. sulcinodis, M. specioides and M. schencki are used as secondary hosts. Possible explanations for this highly variable host use include (1) regional differences in semiochemicals, behaviour or social structure of the potential Myrmica host species and (2) the existence of different ecological subspecies or cryptic species of M. rebeli. Finally, we emphasize the importance of identifying local host ant species prior to further conservation strategies in order to avoid failure of management programs or even damage to populations on the edge of extinction.
Parasitic relationships between lycaenid butterfly larvae and ants are contrasted with the more common, and ancestral, mutualistic butterfly-ant associations. Three types of lycaenid-ant parasitism can be recognized: (i) the Miletinae type (derived from predation on Homoptera); (ii) the Aphnaeini type (derived from obligate and specific mutualism or commensalism); and (iii) the Maculinea type (derived from facultative mutualism, only represented by the genera Maculinea and Lepidochrysops). Parasitic lycaenid-ant interactions are rare (37 confirmed recorded cases worldwide) and are mostly confined to single species, or small species-groups, in larger non-parasitic clades. Only the two genera representing the Maculinea type have undergone substantial radiation. Ant-parasitic lycaenids predominantly occur in highly seasonal habitats with an extended unfavourable dry or cold season. These observations suggest that (a) parasitic interactions are relatively unstable in evolutionary time, and (b) their evolution usually started with caterpillars seeking shelter in ant nests. Ecological and zoogeographical data for species of the Glaucopsychiti (of which Maculinea forms a part) are compiled and used to discuss the evolutionary origin of ant-parasitism in Maculinea butterflies in a comparative framework. These comparisons suggest that (a) Maculinea evolved from facultative unspecific ant-mutualists, (b) the loss of larval tentacle organs is primarily related to their endophytic feeding habits, (c) that Lamiaceae were the hostplants of ancestral Maculinea, and (d) that Maculinea evolved in eastern central Asia. Further phylogenetic and biogeographical analyses are required to quantitatively test these possibilities. Rapid Science Ltd. 1998
Maculinea butterflies in Europe, and probably most of Asia, are host specific social parasites of various species of Myrmica ants. The latest summary of field data showing the pattern of host specificity by Maculinea is presented. Myrmica ants have been well studied in the laboratory but much less is known about the ecology of their natural populations. While the former is important in understanding the adaptive evolution of Maculinea larval behaviours, the latter is of more practical importance to conservationists charged with the protection of specific populations of Maculinea. The current knowledge of habitat partition, colony growth and colony reproduction within communities of Myrmica ants is summarized in relation to the ecology of Maculinea species. Concepts used in current population simulation models are explained. A key concept is the idea that community structure (both number of species and size and abundance of nests) is controlled by the quantity and quality of suitable nest sites. Some advice is given to conservationists who might need to manipulate Myrmica ant populations in order to maintain a robust population of a Maculinea species. Rapid Science Ltd. 1998
Maculinea butterflies show social parasitism via obligatory myrmecophily as their larvae are adopted and raised to pupation by Myrmica ants. Suitable hosts differ for different Maculinea species, and host ant specificity can further differ at the population-level. Although early studies suggested single ant
species as main hosts for each Maculinea species, it has recently become clear that their host ant specificity is more complex. Maculinea alcon and Maculinea ‘rebeli’ have variously been separated according to adult and larval morphology, phenology, and their use of different ecosystems,
including host plant and host ant species. However, recent genetic evidence has questioned their separation as good species.
Here we compare the use of host ants by M. alcon and M. ‘rebeli’ at the regional scale in NE-Hungary and Transylvania (Romania), where molecular studies have found no species-level separation
between the two forms. We opened 778 nests of Myrmica ants and searched for Maculinea specimens (larvae, pupae and exuviae) shortly before imago emergence from the nest in seven M. alcon sites, six M. ‘rebeli’- sites and one site where both M. alcon and M. ‘rebeli’ are syntopic. In all, Maculinea caterpillars were found in the nests of seven different ant species (M. alcon was recorded mainly with Myrmica scabrinodis and occasionally with M. salina and M. vandeli; M. ‘rebeli’ used mainly M. scabrinodis, M. sabuleti and M. schencki and occasionally M. lonae and M. specioides). Myrmica scabrinodis was found to be a general host of both M. alcon and M. ‘rebeli’, which is the first record for a common host ant of these two closely related butterflies within the same region. However
there were also differences in host ant use patterns between the sites occupied by the two Maculinea taxa, which reflect differences in Myrmica communities between the two types of habitat. Possible explanations for the similar but not identical host use patterns of
M. alcon and M. ‘rebeli’, and their relevance for the question of whether they are separate species are discussed.
Although it has always been assumed that chemical mimicry and camouflage play a major role in the penetration of ant societies by social parasites, this paper provides the first direct evidence for such a mechanism between the larvae of the parasitic butterfly Maculinea rebeli and its ant host Myrmica schencki. In the wild, freshly moulted fourth-instar caterpillars, which have no previous contact with ants, appear to be recognized as ant larvae by foraging Myrmica workers, which return them to their nest brood chambers. Three hypotheses concerning the mechanism controlling this behaviour were tested: (i) the caterpillars produce surface chemicals that allow them to be treated as ant larvae; (ii) mimetic compounds would include hydrocarbons similar to those employed by Myrmica to recognize conspecifics and brood; and (iii) the caterpillars' secretions would more closely mimic the profile of their main host in the wild, M. schencki, than that of other species of Myrmica. Results of behavioural bioassays and chemical analyses confirmed all three hypotheses, and explained the high degree of host specificity found in this type of highly specialized myrmecophile. Furthermore, although caterpillars biosynthesized many of the recognition pheromones of their host species (chemical mimicry), they later acquired additional hydrocarbons within the ant nest (chemical camouflage), making them near-perfect mimics of their individual host colony's odour.
Ants dominate terrestrial ecosystems through living in complex societies whose organization is maintained via sophisticated
communication systems. The role of acoustics in information exchange may be underestimated. We show that Myrmica schencki queens generate distinctive sounds that elicit increased benevolent responses from workers, reinforcing their supreme social
status. Although fiercely defended by workers, ant societies are infiltrated by specialist insects that exploit their resources.
Sounds produced by pupae and larvae of the parasitic butterfly Maculinea rebeli mimic those of queen ants more closely than those of workers, enabling them to achieve high status within ant societies.
We conclude that acoustical mimicry provides another route for infiltration for ∼10,000 species of social parasites that cheat
ant societies.
A polymorphism in growth rates was recently described affecting the larval development of the myrmecophilous butterfly Maculinea rebeli, spanning different years in a single insect population. The close integration of M. rebeli into the host ant colonies, facilitated by adaptations in behaviour and chemical mimicry, make extended larval development a successful strategy. Here we present additional data for M. rebeli and new data for Maculinea alcon (another cuckoo-feeding lycaenid) and the two myrmecophilous predators Maculinea arion and Microdon mutabilis (Diptera: Syrphidae). As predicted, M. alcon shows the same growth pattern as M. rebeli with a proportion of caterpillars developing in one year and the remainder over two years. This pattern holds in both northern and southern European populations, where M. alcon exploits different species of host. Against expectation, the same bimodal distribution of pre-pupation body weights, indicating one and two year developers, was found for the larvae of M. arion and M. mutabilis. As predators, both species are less closely integrated in their host ant colonies, suggesting that the polymorphism in growth rates is a more general adaptation to a myrmecophilous life style, arrived at by convergent evolution between the Maculinea and Microdon species. For predatory species we suggest that biennialism is an adaptation to the migratory behaviour of the host made possible by the predators' ability to fast over extended periods. We also hypothesize that M. arion represents an ancestral strategy in Maculinea butterflies and that the growth polymorphism might have become genetically fixed in the cuckoo-feeding species.
The chemical strategies by which parasites manage to break into the social fortresses of ants offer a fascinating theme in chemical ecology. Semiochemicals used for interindividual nestmate recognition are also involved in the mechanisms of tolerance and association between the species, and social parasites exploit these mechanisms. The obligate parasites are odorless ("chemical insignificance") at the time of usurpation, like all other callow ants, and this "invisibility" enables their entry into the host colony. By chemical mimicry (sensu lato), they later integrate the gestalt odor of this colony ("chemical integration"). We hypothesize that host and parasite are likely to be related chemically, thereby facilitating the necessary mimicry to permit bypassing the colony odor barrier. We also review the plethora of chemical weapons used by social parasites (propaganda, appeasement, and/or repellent substances), particularly during the usurpation period, when the young mated parasite queen synthesizes these chemicals before usurpation and ceases such biosynthesis afterwards. We discuss evolutionary trends that may have led to social parasitism, focusing on the question of whether slave-making ants and their host species are expected to engage in a coevolutionary arms race.
Large blue (Maculinea) butterflies are highly endangered throughout the Palaearctic region, and have been the focus of intense conservation research. In addition, their extraordinary parasitic lifestyles make them ideal for studies of life history evolution. Early instars consume flower buds of specific host plants, but later instars live in ant nests where they either devour the brood (predators), or are fed mouth-to-mouth by the adult ants (cuckoos). Here we present the phylogeny for the group, which shows that it is a monophyletic clade nested within Phengaris, a rare Oriental genus whose species have similar life histories. Cuckoo species are likely to have evolved from predatory ancestors. As early as five million years ago, two Maculinea clades diverged, leading to the different parasitic strategies seen in the genus today. Contrary to current belief, the two recognized cuckoo species show little genetic divergence and are probably a single ecologically differentiated species. On the other hand, some of the predatory morphospecies exhibit considerable genetic divergence and may contain cryptic species. These findings have important implications for conservation and reintroduction efforts.
Large blue butterflies are notable for their rarity and ability to dupe ants, and they are endangered. A genetic reconstruction of how social parasitism evolved among them will overturn conservation priorities.
The presence of annual and biennial individuals within the same population has been recently demonstrated in the myrmecophilous butterflies Maculinea rebeli and Maculinea alcon, which present a cuckoo strategy inside Myrmica nests, and Maculinea arion which is a predatory species. Here, we present field and laboratory data on polymorphic larval growth in two other predatory species of Maculinea: M. teleius and M. nausithous. Body mass distributions of pre-pupation larvae were bimodal in both species. These results point to the existence of larvae that develop in 1 or 2 years. We also showed that the probability of pupation depended on larval body mass. In the case of M. teleius, the critical body mass at which larvae have a 50% probability of pupation is about 80 mg. We suggest that polymorphism in Maculinea may have evolved as an adaptation to life in ant nests, a habitat which protects them from predators and provides food. However, the quality of this resource is highly variable and unpredictable. According to the bet-hedging hypothesis, if the habitat is unpredictable, females should have an advantage by producing more variable offspring. In the case of Maculinea butterflies, this may involve maintaining larvae that develop in 1 or 2 years.
A discrete-time host-parasitoid model including host-density dependence and a generalized Thompson escape function is analyzed. This model assumes that parasitoids are egg-limited but not search-limited, and is proven to exhibit five types of dynamics: host failure in which the host goes extinct in the parasitoid's presence or absence, unconditional parasitoid failure in which the parasitoid always goes extinct while the host persists, conditional parasitoid failure in the host and the parasitoid go extinct or coexist depending on the initial host-parasitoid ratio, parasitoid driven extinction in which the parasitoid invariably drives the host to extinction, and coexistence in which the host and parasitoid coexist about a global attractor. The latter two dynamics only occur when the parasitoid's maximal rate of growth exceeds the host's maximal rate of growth. Moreover, coexistence requires parasitism events to be sufficiently aggregated. Small additive noise is proven to alter the dynamical outcomes in two ways. The addition of noise to parasitoid driven extinction results in random outbreaks of the host and parasitoid with varying intensity. Additive noise converts conditional parasitoid failure to unconditional parasitoid failure. Implications for classical biological control are discussed.
Mechanisms of recognition are essential to the evolution of mutualistic and parasitic interactions between species. One such
example is the larval mimicry that Maculinea butterfly caterpillars use to parasitize Myrmica ant colonies. We found that the greater the match between the surface chemistry of Maculinea alcon and two of its host Myrmica species, the more easily ant colonies were exploited. The geographic patterns of surface chemistry indicate an ongoing coevolutionary
arms race between the butterflies and Myrmica rubra, which has significant genetic differentiation between populations, but not between the butterflies and a second, sympatric
host, Myrmica ruginodis, which has panmictic populations. Alternative hosts may therefore provide an evolutionary refuge for a parasite during periods
of counteradaptation by their preferred hosts.
1. The five European species of Maculinea butterflies are among the most endangered invertebrates in the world. To attain a better understanding of the mechanisms which are most influential to their population dynamics, we develop a mathematical population model for one of these species, Maculinea rebeli, based on its dependence on two sequential resources, the cross-leaved gentian, Gentiana cruciata, and a red ant, Myrmica schencki. One of the main objects of this modelling study is to raise questions about the ecology and conservation of this rare and fascinating butterfly. 2. The model has two main biological components: (i) recruitment and competition on the plant for the first few weeks of butterfly life, and (ii) recruitment by and competition within nests of the red ant for the remainder of the butterfly life-cycle. 3. We estimate all of the parameters for the model based in part on data collected at a 4-ha study site in the Spanish Pyrénées, one of the largest known populations of Maculinea in the world. 4. The model is used to evaluate how different ecological processes and densities of the plant and ant resources may affect the butterfly population, including its density, resilience from perturbation, and persistence. 5. The model clearly indicates that, for the Spanish study site, the survival of the butterfly in ant nests is disproportionately more important to its population than is competition on the plant. Changes in the observed population of the plant have virtually no impact on the butterfly population. 6. Future studies should take account for instance of changes in the density of ant nests and the population of a specialist ichneumonid parasitoid.
Fourth instar larvae of Maculinea species of lycaenid butterfly live as social parasites insideMyrmica ant nests. They show highly unusual growth patterns, with small but regular growth in early phytophagous instars, followed by >10 times the growth predicted by extrapolating the early growth rate (following Dyar's rule) during the final carnivorous instar. This produces striking allometry between head and body size in full-grown larvae (ratios of 4–5% compared with 8–10%). Larvae of the Myrmica ant hosts have a similar growth. Data for c. 150 other lycaenid species showed that species with similar life-histories exhibit the same unusual growth pattern (Phengaris sppLepidochrysops spp Niphanda fusca); all others have regular growth throughout their larval life, including the carnivorous species that are parasitic on ants from the first instar. It is suggested that Maculinea -type growth pattern has arisen convergently in at least three unrelated lineages of lycaenids. Selection pressures might include the need for reduced early growth to produce late instars that are small enough to be integrated as brood mimics into ant social systems, combined with the need to achieve at least the same adult size as the ancestral species. Trophic pressures that operate on both sedentary ant and butterfly larvae, which must survive long periods of starvation and grow rapidly when food is abundant, may also be involved.
(1) Population data for colonies of Myrmica rubra L., collected in two manners, are analysed and compared with special reference to the density of queens in colonies. (2) The Leslie & Gower model for host/parasite relationships is adopted to describe the growth of worker and queen populations of M. rubra as interacting systems. (3) Values for the parameters are proposed and data from simulations are given to illustrate how the model can be interpreted in terms of ant biology. It has been found that this model can reproduce the observed data quite well.
1. Caterpillars of the butterfly, Maculinea rebeli, feed sequentially in flower-buds of Gentiana cruciata and in nests of Myrmica schencki ants, with which they have a sort of 'cuckoo bird' relationship. Ants feed them in preference to their own larvae, reducing the production of new workers and hence the colony size the following year. 2. Other Myrmica compete with M. schencki for nest-sites. They adopt caterpillars with equal facility, but fail to rear them to maturity and are consequently less damaged. 3. Using a mathematical model we explore how species interactions can influence the populations of the butterfly, M. schencki, and other Myrmica species. The model assumes a 1 ha square of 900 cells with a fixed population of gentians. A cell can contain at most a single Myrmica colony which can adopt a proportion of the caterpillars leaving the gentians. Both density-dependent and density-independent butterfly mortalities occur on the plant and within the nest. 4. M. schencki is more successful in hotter, drier habitat patches than other Myrmica. This is simulated by a one-dimensional gradient in the maximum yearly reproductive rate (R) of M. schencki, the gradient for other Myrmica species being approximately reciprocal to that of M. schencki. M. schencki and other Myrmica compete pre-emptively for vacant nest sites. 5. The model is seeded with nests and run for 50 generations, to stabilize the ant distributions, before being 'colonized' by a single female of Maculinea rebeli. Addition of the butterfly to the system reduces dramatically both the number and average size of M. schencki nests. As a result, the number of nests of other Myrmica increases as they encroach onto the drier areas. In intermediate areas, where most pre-emptive competition occurs, the nest-size of other Myrmica increases, but overall, their average size also falls because of the direct effect of the caterpillars. 6. The system stabilizes at about 268 nests of M. schencki, 73% being in cells containing G. cruciata and so able to adopt caterpillars and 27% being in plant-free cells, avoiding parasitization. Only 16% of cells are plant-free, demonstrating the negative effect of the butterfly on the spatial distribution of M. schencki and its ability to mediate apparent competition between plants and ants. 7. The model predicts that: (a) the largest populations of butterflies should occur in systems of intermediate plant density (c. 1000-1500 plants ha-1); (b) the greatest turnover in ant nests should occur in dryer areas, where nests of M. schencki are relatively most damaged by the butterfly, despite a pronounced impact on the ant populations in the first years following colonization; (c) only c. 0.2% of nests should go extinct each subsequent year as a consequence of butterfly parasitization; and (d) only about half of the potential rearing capacity of the M. schencki population should be exploited by the butterfly in any one year. 8. We suggest that a subtle combination of changes in the environment can either benefit or endanger the butterfly population depending on how each of the ant species are affected. 9. From a conservation stand-point, population size is not necessarily an accurate predictor of the fragility of the butterfly population; as long as the butterfly population is safe from stochastic mechanisms of local extinction, the intrinsic and resource-based components of the butterflies' basic reproductive rate are better indicators of persistence.
Europe's five species ofMaculinea butterfly are examples of endangered species adapted to live in traditional, cultural landscapes. All are threatened with extinction in Western Europe because of recent changes in land use. This is illustrated by an historical account of the extinction of the BritishMaculinea arion populations, despite many conservation attempts. It is shown how the failures proved to be due to ignorance of the key factor forM. arion, its specialization on a single ant host,Myrmica sabuleti. A brief account is given of research that shows how each of the five species is similarly dependent upon a separate hostMyrmica ant species and how each has an interesting and rare specific parasitoid. Steps for the practical conservation of existingMaculinea populations including the obligation, under the Bern Convention, to re-establish nationally extinct species are outlined. The procedure and problems involved in re-establishment are illustrated with reference to the successful programme forM. arion in Britain. The best way of ensuring robust populations ofMaculinea butterflies is to manage habitats to optimize the density and distribution of the required species ofMyrmica host and, secondarily, the distribution of the larval food plant. The value of single species conservation in cultural habitats is discussed. It is concluded that this is possible to achieve and that other rare organisms also often benefit, but only when conservation measures are based on the results of detailed autecological research.
Multihost parasites can infect different types of hosts or even different host species. Epidemiological models have shown the importance of the diversity of potential hosts for understanding the dynamics of infectious disease (e.g., the importance of reservoirs), but the consequences of this diversity for virulence and transmission evolution remain largely overlooked. Here, I present a general theoretical framework for the study of life-history evolution of multihost parasites. This analysis highlights the importance of epidemiology (the relative quality and quantity of different types of infected hosts) and between-trait constraints (both within and between different hosts) to parasite evolution. I illustrate these effects in different transmission scenarios under the simplifying assumption that parasites can infect only two types of hosts. These simple but contrasted evolutionary scenarios yield new insights into virulence evolution and the evolution of transmission routes among different hosts. Because many of the pathogens that have large public-health and agricultural impacts have complex life cycles, an understanding of their evolutionary dynamics could hold substantial benefits for management.
Continuous-trait game theory fills the niche of enabling analytically solvable models of the evolution of biologically realistically complex traits. Game theory provides a mathematical language for under- standing evolution by natural selection. Continuous-trait game the- ory starts with the notion of an evolutionarily stable strategy (ESS) and adds the concept of convergence stability (that the ESS is an evo- lutionary attractor). With these basic tools in hand, continuous-trait game theory can be easily extended to model evolution under con- ditions of disruptive selection and speciation, nonequilibrium pop- ulation dynamics, stochastic environments, coevolution, and more. Many models applying these tools to evolutionary ecology and co- evolution have been developed in the past two decades. Going for- ward we emphasize the communication of the conceptual simplicity and underlying unity of ideas inherent in continuous-trait game the- ory and the development of new applications to biological questions.
Fourth instar larvae of Maculinea species of lycaenid butterfly live as social parasites inside Myrmica ant nests. They show highly unusual growth patterns, with small but regular growth in early phytophagous instars, followed by >10 times the growth predicted by extrapolating the early growth rate (following Dyar's rule) during the final carnivorous instar. This produces striking allometry between head and body size in full-grown larvae (ratios of 4–5% compared with 8–10%). Larvae of the Myrmica ant hosts have a similar growth. Data for c. 150 other lycaenid species showed that species with similar life-histories exhibit the same unusual growth pattern (Phengaris spp., Lepidochrysops spp., Niphanda fused); all others have regular growth throughout their larval life, including the carnivorous species that are parasitic on ants from the first instar. It is suggested that Maculinea-type growth pattern has arisen convergently in at least three unrelated lineages of lycaenids. Selection pressures might include the need for reduced early growth to produce late instars that are small enough to be integrated as brood mimics into ant social systems, combined with the need to achieve at least the same adult size as the ancestral species. Trophic pressures that operate on both sedentary ant and butterfly larvae, which must survive long periods of starvation and grow rapidly when food is abundant, may also be involved.
1. Field studies were made of the benefits and costs of two feeding strategies in the genus Maculinea, whose final-instar larvae parasitise Myrmica ant colonies. Maculinea arion is an obligate predator of ant brood, whereas M. rebeli and M. alcon mimic ant larvae and are fed (like cuckoos) directly by the workers.
2. Samples of > 1500 Myrmica nests confirmed laboratory-based predictions that, by feeding at a lower trophic level, many (4.7-fold) more individuals of M. rebeli and M. alcon are supported per ant colony than M. arion.
3. Because of their efficient feeding, cuckoo species often occupied sites where their phytophagous early larval populations coincided to only a small extent (> 10%) with host Myrmica colonies, whereas all sites supporting M. arion had 50–100% of the phytophagous stages within foraging range of the host Myrmica species.
4. Greater host-specificity was identified as another consequence of cuckoo-feeding. The ecological cost of this is discussed.
5. The feeding of other Maculinea species had not been fully described: the data suggest that M. nausithous is a predator of ant brood and confirm that M. teleius is predacious.
The relationship between behavioural tests and relative proportions of cuticular components were studied in the slave-making species Polyergus rufescens and the slave and Formica rufibarbis living in either monospecific or mixed colonies. A correlation between the relative proportions of the cuticular products and interindividual recognition exists in each of the two species Polyergus and Formica: Polyergus are fiercely aggressive towards individuals which have different cuticular spectra and originate from a geographically isolated nest. This seems to be true also in the case of Formica living in monospecific colonies. A similar correlation also exists between the two species, which have different cuticular spectra: encounters arranged between them show that free-living Formica are always fiercely aggressive towards Polyergus. The reason why no such correlation seems to exist, however, between Polyergus and Formica when the latter are enslaved and the two species coexist peacefully at the same nest is discussed.
Caterpillars of Maculinea arion are obligate predators of the brood of Myrmica sabuleti ants. In the aboratory, caterpillars eat the largest available ant larvae, although eggs, small larvae and prepupae are also palatable. This is an efficient way to predate. It ensures that newly-adopted caterpillars consume the final part of the first cohort of ant brood in a nest, before this pupates in early autumn and becomes unavailable as prey. At the same time, the fixed number of larvae in the second cohort is left to grow larger before being killed in late autumn and spring. Caterpillars also improve their feeding efficiency by hibernating for longer than ants in spring, losing just 6% of their weight while the biomass of ant larvae increases by 27%. Final instar caterpillars acquire more than 99% of their ultimate biomass in Myrmica nests, growing from 1.3 mg to an estimated 173 mg. A close correlation was found between the weights of caterpillars throughout autumn and the number of large ant larvae they had eaten. This was used to calculate the number of larvae eaten in spring, allowing both for the loss of caterpillar weight during winter and the increase in the size of their prey in spring. It is estimated that 230 of the largest available larvae, and a minimum nest size of 354 M. sabuleti workers, is needed to support one butterfly. Few wild M. sabuleti nests are this large: on one site, it was estimated that 85% of nests were too small to produce a butterfly, and only 5% could support two or more. This prediction was confirmed by the mortalities of 376 caterpillars in 151 wild M. sabuleti nests there. Mortalities were particularly high in nests that adopted more than two caterpillars, apparently due to scramble competition and starvation in autumn. Survival was higher than predicted in wild nests that adopted one caterpillar. These caterpillars seldom exhaust their food before spring, when there is intense competition among Myrmica for nest sites. Ants often desert their nests in the absence of brood, leaving the caterpillar behind. Vacant nests are frequently repopulated by a neighbouring colony, carrying in a fresh supply of brood. Maculinea arion caterpillars have an exceptional ability to withstand starvation, and sometimes survive to parasitize more than one Myrmica colony. Despite these adaptations, predation is an inefficient way to exploit the resources of a Myrmica nest. By contrast, Maculinea rebeli feeds mainly at a lower trophic level, on the regurgitations of worker ants. Published data show that Myrmica nests can support 6 times more caterpillars of Maculinea rebeli than of M. arion in the laboratory. This is confirmed by field data.
Ecological studies have been made of all 5 European species of Maculinea. These confirm that M. nausithous and M. rebeli live underground in Myrmica ant nests for 10 months of the year, as has long been known for the other 3 species. The main discovery was that each Maculinea species depends on a single, and different, host species of Myrmica. This specificity contradicts previous papers and scientific reviews of the relationship between Maculinea and ants. Therefore, early records are re-examined and 3 reasons are given to explain why most are misleading when applied to wild populations. Dependence on a single, rather than any, species of Myrmica explains why Maculinea populations exist in only a small minority of biotopes where their foodplants and Myrmica ants abound. It also explains the puzzling disappearance of Maculinea populations from apparently suitable sites. The discovery that M. alcon and M. rebeli depend on separate species of Myrmica that are not even closely related strengthens the argument that these butterflies are good species.
Maculinea butterflies are parasites of Myrmica ant nests. The Alcon blue,Maculinea alcon , is unusual in that it parasitizes the nests of several Myrmica species, usingM. rubra, M. ruginodis and M. scabrinodis as hosts in different parts of Europe. In Denmark it uses M. rubra and M. ruginodis, but never M. scabrinodis. Some populations use one of these species exclusively, despite the presence of the alternative host, while others use both hosts simultaneously. To examine the basis of this specificity, and local coadaptation between host and parasite, we offered freshly emerged caterpillars ofM. alcon from three populations differing in their host use to laboratory nests of all three recorded host ant species collected from each of the M. alcon populations. We measured the attractiveness of the caterpillars to their host ants as the time taken for them to be adopted by each ant colony. Caterpillars from all populations took longer to be adopted to M. scabrinodis nests than to nests of the other two ant species. Adoption times toM. rubra and M. ruginodis colonies differed: caterpillars from each of the two populations that used a single host species were adopted most quickly by that species when local ant colonies were used. When ant colonies collected from the other two sites were used, this pattern broke down, and there was either no difference in adoption time, orM. rubra adopted caterpillars more quickly. Adoption of caterpillars from the population that used bothM. rubra and M. ruginodis as hosts took an order of magnitude longer than caterpillars from populations using a single host species.
Many host species interact with a specific parasite within only a fraction of their geographical range. Where host and parasite overlap geographically, selection may be reciprocal constituting a coevolutionary hot spot. Host evolution, however, may be driven primarily by selection imposed by alternative biotic or abiotic factors that occur outside such hot spots. To evaluate the importance of coevolutionary hot spots for host and parasite evolution, we analyse a spatially explicit genetic model for a host that overlaps with a parasite in only part of its geographical range. Our results show that there is a critical amount of overlap beyond which reciprocal selection leads to a coevolutionary response in the host. This critical amount of overlap depends upon the explicit spatial configuration of hot spots. When the amount of overlap exceeds this first critical level, host-parasite coevolution commonly generates stable allele frequency clines rather than oscillations. It is within this region that one of the primary predictions of the geographic mosaic theory is realized, and local maladaptation is prevalent in both species. Past a further threshold of overlap between the species oscillations do evolve, but allele frequencies in both species are spatially synchronous and local maladaptation is absent in both species. A consequence of such transitions between coevolutionary dynamics is that parasite adaptation is inversely proportional to the fraction of its host's range that it occupies. Hence, as the geographical range of a parasite increases, it becomes increasingly maladapted to the host. This suggests a novel mechanism through which the geographical range of parasites may be limited.
Multihost parasites can infect different types of hosts or even different host species. Epidemiological models have shown the importance of the diversity of potential hosts for understanding the dynamics of infectious disease (e.g., the importance of reservoirs), but the consequences of this diversity for virulence and transmission evolution remain largely overlooked. Here, I present a general theoretical framework for the study of life-history evolution of multihost parasites. This analysis highlights the importance of epidemiology (the relative quality and quantity of different types of infected hosts) and between-trait constraints (both within and between different hosts) to parasite evolution. I illustrate these effects in different transmission scenarios under the simplifying assumption that parasites can infect only two types of hosts. These simple but contrasted evolutionary scenarios yield new insights into virulence evolution and the evolution of transmission routes among different hosts. Because many of the pathogens that have large public-health and agricultural impacts have complex life cycles, an understanding of their evolutionary dynamics could hold substantial benefits for management.
Between major pandemics, the influenza A virus changes its antigenic properties by accumulating point mutations (drift) mainly in the RNA genes that code for the surface proteins hemagglutinin (HA) and neuraminidase (NA). The successful strain (variant) that will cause the next epidemic is selected from a reduced number of progenies that possess relatively high transmissibility and the ability to escape from the immune surveillance of the host. In this paper, we analyse a one-dimensional model of influenza A drift (Z. Angew. Math. Mech. 76 (2) (1996) 421) that generalizes the classical SIR model by including mutation as a diffusion process in a phenotype space of variants. The model exhibits traveling wave solutions with an asymptotic wave speed that matches well those obtained from numerical simulations. As exact solutions for these waves are not available, asymptotic estimates for the amplitudes of infected and recovered classes are provided through an exponential approximation based on the smallness of the diffusion constant. Through this approximation, we find simple scaling properties to several parameters of relevance to the epidemiology of the disease.
We develop and analyze an explicit multilocus genetic model of coevolution. We assume that interactions between two species (mutualists, competitors, or victim and exploiter) are mediated by a pair of additive quantitative traits that are also subject to direct stabilizing selection toward intermediate optima. Using a weak-selection approximation, we derive analytical results for a symmetric case with equal locus effects and no mutation, and we complement these results by numerical simulations of more general cases. We show that mutualistic and competitive interactions always result in coevolution toward a stable equilibrium with no more than one polymorphic locus per species. Victim-exploiter interactions can lead to different dynamic regimes including evolution toward stable equilibria, cycles, and chaos. At equilibrium, the victim is often characterized by a very large genetic variance, whereas the exploiter is polymorphic in no more than one locus. Compared to related one-locus or quantitative genetic models, the multilocus model exhibits two major new properties. First, the equilibrium structure is considerably more complex. We derive detailed conditions for the existence and stability of various classes of equilibria and demonstrate the possibility of multiple simultaneously stable states. Second, the genetic variances change dynamically, which in turn significantly affects the dynamics of the mean trait values. In particular, the dynamics tend to be destabilized by an increase in the number of loci.
Coevolution is a major process operating across biological communities at a range of spatial scales. Rapid ecological change makes it vital that we understand how coevolution proceeds if we are to conserve genetic diversity, combat disease and predict the effects of species invasions.
Multilocus genetics and the coevolution of quantitative traits Evolutionary game theory and adaptive dynamics of continuous traits
- M Kopp
- S Gavrilets
M. Kopp, S. Gavrilets, Multilocus genetics and the coevolution of quantitative traits, Evolution 60 (2006) 1321–1336. [7] B.J. McGill, J.S. Brown, Evolutionary game theory and adaptive dynamics of continuous traits, Annual Review of Ecology, Evolution and Systematics 38 (2007) 403–435.