Increased genetic diversity as a defence against parasites is undermined by social parasites: Microdon mutabilis hoverflies infesting Formica lemani ant colonies.

Genetic diversity can benefit social insects by providing variability in immune defences against parasites and pathogens. However, social parasites of ants infest colonies and not individuals, and for them a different relationship between genetic diversity and resistance may exist. Here, we investigate the genetic variation, assessed using up to 12 microsatellite loci, of workers in 91 Formica lemani colonies in relation to their infestation by the specialist social parasite Microdon mutabilis. At the main study site, workers in infested colonies exhibited lower relatedness and higher estimated queen numbers, on average, than uninfested ones. Additionally, estimated queen numbers were negatively correlated with estimated average numbers of mates per queen within infested colonies. At another site, infested colonies also exhibited significantly lower worker relatedness, and estimated queen numbers were comparable in trend. In contrast, in two populations of F. lemani where M. mutabilis was absent, relatedness within colonies was high (40 and 90% with R>0.6). While high genetic variation can benefit social insects by increasing their resistance to pathogens, there may be a cost in the increased likelihood of infiltration by social parasites owing to greater variation in nestmate recognition cues. This study provides the first empirical test of this hypothesis.

Host propagation permits extreme local adaptation in a social parasite of ants.

The Red Data Book hoverfly species Microdon mutabilis is an extreme specialist that parasitises ant societies. The flies are locally adapted to a single host, Formica lemani, more intimately than was thought possible in host-parasite systems. Microdon egg survival plummeted in F. lemani colonies > 3 km away from the natal nest, from c. 96% to 0% to < 50%, depending on the hoverfly population. This is reflected in the life-time dispersal of females, measured at < 2 m, resulting in oviposition back into the same ant nests for generation after generation. To counter destabilizing effects on the host, Microdon manipulates the social dynamics of F. lemani by feeding selectively on ant eggs and small larvae, which causes surviving larvae to switch development into queens. Infested colonies rear double the number of new queens, thus propagating the vulnerable local genotype and compensating for damage to the host colonies. The consequences of such extreme host specificity for insect conservation are discussed.

Changes in chemical signature and host specificity from larval retrieval to full social integration in the myrmecophilous butterfly Maculinea rebeli.

The ant social parasite, Maculinea rebeli shows high levels of host specificity at a regional scale. While 68-88% of caterpillars in the field are adopted by nonhost Myrmica ants, 95-100% of the butterflies emerge from the natural host M. schencki the following year. While retrieval of preadoption caterpillars is specific to the genus Myrmica, it does not explain differential survival with different Myrmica species. We present survival data with host and nonhost Myrmica species suggesting that, with nonhosts (M. sabuleti and M. rubra), survival depends on the physiological state of the colony. We also compared the similarities of the epicuticular surface hydrocarbon signatures of caterpillars that were reared by host and nonhost Myrmica for 3 weeks with those from tending workers. Counterintuitively, the hydrocarbons of postadoption caterpillars were more similar (78%, 73%) to the ant colony profiles of the nonhost species than were caterpillars reared in colonies of M. schencki (42% similarity). However, caterpillars from M. schencki nests that were then isolated for 4 additional days showed unchanged chemical profiles, whereas the similarities of those from nonhost colonies fell to 52 and 56%, respectively. Six compounds, presumably newly synthesized, were detected on the isolated caterpillars that could not have been acquired from M. sabuleti and M. rubra (nor occurred on preadoption caterpillars), five of which were found on the natural host M. schencki. These new compounds may relate to the high rank the caterpillars attain within the hierarchy of M. schencki societies. The same compounds would identify the caterpillars as intruders in non-schencki colonies, where their synthesis appeared to be largely suppressed. The ability to synthesize or suppress additional compounds once adopted explains the pattern of mortalities found among fully integrated caterpillars in Myrmica colonies of different species and physiological states.

Parasitoid secretions provoke ant warfare.

Insect social parasites are extreme specialists that typically use mimicry or stealth to enter ant colonies to exploit the rich, but fiercely protected, resources within their nests. Here we show how a parasitic wasp (parasitoid) contrives to reach its host, itself an endangered species of social parasite that lives inside the brood chambers of ant nests, by releasing semiochemicals to induce in-fighting between worker ants, locking the colony in combat and leaving it underprotected. Four of these chemicals are new to biology and have the potential to control pest species by inducing different agonistic behaviours in ants.

Food-plant niche selection rather than the presence of ant nests explains oviposition patterns in the myrmecophilous butterfly genus Maculinea.

It has been suggested that the socially parasitic butterfly Maculinea alcon detects ant odours before ovipositing on initial larval food plants near colonies of its obligate ant host Myrmica ruginodis. It has also been suggested that overcrowding on food plants near M. ruginodis is avoided by an ability to detect high egg loads, resulting in a switch to selecting plants near less suitable ant species. If confirmed, this hypothesis (H1) would have serious implications for the application of current population models aimed at the conservation of endangered Maculinea species, which are based on the null hypothesis (H0) that females randomly select food plants whose flower buds are at a precise phenological stage, making oviposition independent of ants. If H1 were wrong, practical management based upon its assumptions could lead to the extinction of protected populations. We present data for the five European species of Maculinea which show that (i) each oviposits on a phenologically restricted flower-bud stage, which accounts for the apparent host-ant-mediated niche separation in sympatric populations of Maculinea nausithous and Maculinea teleius, (ii) there is no temporal shift in oviposition by Maculinea arion in relation to host ant distribution or egg density, and (iii) oviposition patterns in 13 populations of M. alcon's closest relative, Macaulinea rebeli, conform to H0 not H1 predictions. It is concluded that conservation measures should continue to be based on H0.

Polymorphic growth rates in myrmecophilous insects.

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.

Respiratory Q10 varies between populations of two species of Myrmica ants according to the latitude of their sites.

Metabolic respiration by groups of resting Myrmica ruginodis and M. scabrinodis worker ants from five sites representing a range of latitudes, have been compared by measuring rates of CO(2) production-standardised by fat-free weight-at 5 and 25 degrees C. M. ruginodis which lives in cooler habitats than M. scabrinodis consistently produced more CO(2). At 5 degrees C ants of both species from southern latitudes were metabolically more active than those from more northerly latitudes, whereas at 25 degrees C the situation was reversed. Estimates of Q10 were positively correlated with latitude indicating that the respiratory metabolism of northern populations increases relatively more in response to rising temperatures than southern populations. Values of Q10 at different latitudes were the same for both species. The results are discussed in terms of seasonal fluctuations of temperature at different latitudes.

Host specificity among Maculinea butterflies in Myrmica ant nests.

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.

Colony populations of myrmica sulcinodis Nyl. (Hym. Formicidae).

Forty nests of the ant Myrmica sulcinodis Nyl. were collected from Tulloch Moor, Inverness-shire. The populations of workers and sexuals were counted and various morphometric measurements made.50% of the colonies had a queen, small colonies did not produce sexuals while males were produced mainly by large queenless colonies and gynes by large queened colonies. The data suggests that M. sulcinodis is a true monogynous species that only produces sexuals towards the end of the colonys life.