Host specificity pattern and chemical deception in a social parasite of ants

Casacci, Luca Pietro; Schönrogge, Karsten; Thomas, J. A.; Balletto, Emilio; Bonelli, Simona

doi:10.1038/s41598-018-38172-4

Cited by 19 publications

(24 citation statements)

References 57 publications

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“…Ovipositing female Maculinea butterflies do, however, select the buds of their food plants that are in particular growth-forms or phenological stages [31,93,99], and these may occur in microhabitats that may be associated with particular Myrmica species [31]. Ideally, therefore, the encounter filter should be the Myrmica community found around food plants on which eggs have been laid [42], although this effect is likely to be small, especially in comparison with difference in Myrmica communities between areas with and without food plants [89,100,101]. On the other hand, females may avoid plants on which others have laid eggs [102], which will lead to a more even distribution of eggs (and larvae) relative to Myrmica nests [94,97].…”

Section: (B) the Encounter Filtermentioning

confidence: 99%

Patterns of host use by brood parasiticMaculineabutterflies across Europe

Tartally

Thomas

Anton

et al. 2019

Phil. Trans. R. Soc. B

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The range of hosts exploited by a parasite is determined by several factors, including host availability, infectivity and exploitability. Each of these can be the target of natural selection on both host and parasite, which will determine the local outcome of interactions, and potentially lead to coevolution. However, geographical variation in host use and specificity has rarely been investigated. Maculinea (= Phengaris ) butterflies are brood parasites of Myrmica ants that are patchily distributed across the Palæarctic and have been studied extensively in Europe. Here, we review the published records of ant host use by the European Maculinea species, as well as providing new host ant records for more than 100 sites across Europe. This comprehensive survey demonstrates that while all but one of the Myrmica species found on Maculinea sites have been recorded as hosts, the most common is often disproportionately highly exploited. Host sharing and host switching are both relatively common, but there is evidence of specialization at many sites, which varies among Maculinea species. We show that most Maculinea display the features expected for coevolution to occur in a geographic mosaic, which has probably allowed these rare butterflies to persist in Europe. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.

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Section: (B) the Encounter Filtermentioning

confidence: 99%

Patterns of host use by brood parasiticMaculineabutterflies across Europe

Tartally

Thomas

Anton

et al. 2019

Phil. Trans. R. Soc. B

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“…Similar strategies were also revealed in non-hymenopteran parasites of Hymenoptera hosts. For example, Casacci et al [28] found that parasitic caterpillars (Phengaris (=Maculinea) rebeli (Hirschke, 1904)) show local variations in host (Myrmica ants) specificity, which are consistent with CHC similarities between hosts and parasites at different sites. Local adaptations in chemical deceptive signals were also detected in the parasitic beetle Meloe franciscanus Van Dyke, 1928 attacking two allopatric populations of Habropoda solitary bees [27].…”

Section: Discussionmentioning

confidence: 87%

“…Because of its low host specialization, however, P. grandior would not be able to chemically match all available hosts at a given location, given that CHC profiles tend to be species-specific in insects [7,13]. In particular, we might document local adaptation to one of the host species as shown in other insect brood parasites, including socially parasitic ants, bee-parasitic beetles and ant-parasitic Lepidoptera [27][28][29]. Alternatively, P. grandior may maintain a weak mimicry to all present hosts and/or reduce the CHC profile complexity and/or CHC amounts (insignificance strategy).…”

Section: Introductionmentioning

confidence: 99%

Low Host Specialization in the Cuckoo Wasp, Parnopes grandior, Weakens Chemical Mimicry but Does Not Lead to Local Adaption

Polidori

Ballesteros

Wurdack

et al. 2020

Insects

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Insect brood parasites have evolved a variety of strategies to avoid being detected by their hosts. Few previous studies on cuckoo wasps (Hymenoptera: Chrysididae), which are natural enemies of solitary wasps and bees, have shown that chemical mimicry, i.e., the biosynthesis of cuticular hydrocarbons (CHC) that match the host profile, evolved in several species. However, mimicry was not detected in all investigated host-parasite pairs. The effect of host range as a second factor that may play a role in evolution of mimicry has been neglected, since all previous studies were carried out on host specialists and at nesting sites where only one host species occurred. Here we studied the cuckoo wasp Parnopes grandior, which attacks many digger wasp species of the genus Bembix (Hymenoptera: Crabronidae). Given its weak host specialization, P. grandior may either locally adapt by increasing mimicry precision to only one of the sympatric hosts or it may evolve chemical insignificance by reducing the CHC profile complexity and/or CHCs amounts. At a study site harbouring three host species, we found evidence for a weak but appreciable chemical deception strategy in P. grandior. Indeed, the CHC profile of P. grandior was more similar to all sympatric Bembix species than to a non-host wasp species belonging to the same tribe as Bembix. Furthermore, P. grandior CHC profile was equally distant to all the hosts’ CHC profiles, thus not pointing towards local adaptation of the CHC profile to one of the hosts’ profile. We conducted behavioural assays suggesting that such weak mimicry is sufficient to reduce host aggression, even in absence of an insignificance strategy, which was not detected. Hence, we finally concluded that host range may indeed play a role in shaping the level of chemical mimicry in cuckoo wasps.

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“…(v) Do larval growth patterns vary between different regions? Although we and colleagues have demonstrated the existence of the growth polymorphism in M. rebeli larvae from the Gap region of the Hautes‐Alpes and the Rhône‐Alpes in France, the Spanish Pyrenees, and the Black Forest, Germany, it is apparently absent from north Italian (Casacci et al ., ) and Hungarian populations (A. Tartally, pers. commun.)…”

Section: Introductionmentioning

confidence: 99%

Evidence of a fixed polymorphism of one‐year and two‐year larval growth in the myrmecophilous butterfly Maculinea rebeli

Elmes

Wardlaw

Schönrogge

et al. 2019

Insect Conserv Diversity

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Maculinea (= Phengaris) species of butterfly have complex life‐styles in which the larvae feed briefly on specific foodplants before entering the final instar, after which they live as social parasites within Myrmica ant colonies and acquire 98–99% of their ultimate biomass by either preying on ant brood (predatory species) or being fed by worker ants (cuckoo species). Cuckoo species demonstrate two growth forms, whereby some individuals develop to pupate in 11 months and others remain 23 months in the nest, a strategy that in theory represents the most efficient exploitation of resources within Myrmica societies. Early studies suggested that development rates in Maculinea rebeli (referred to by other authors as the xerophilous form of Maculinea alcon) were not plastic but represented an unusual fixed polymorphism, in which eggs were genetically predetermined as 1‐ or 2‐year larvae. We tested this idea in lab experiments using M. rebeli from the French Hautes‐Alpes, with these results: (i) the growth strategy of every individual larva is pre‐determined by the mother either genetically or, less probably, during oogenesis. (ii) Intra‐nest competition and host fitness affects survival and growth but does not influence the inherent growth strategy. (iii) The ratio of 1‐ and 2‐year developing larvae is initially about 50:50, although differential survival in crowded nests may alter the ratio of surviving individuals. (iv) All females tested laid eggs that hatched into both 1‐ or 2‐year developers. (v) Growth patterns vary between different regions. Larvae from the Spanish Pyrenees initially grow less than those from the Alps, with a smaller initial differentiation between the size classes.

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Host specificity pattern and chemical deception in a social parasite of ants

Cited by 19 publications

References 57 publications

Patterns of host use by brood parasiticMaculineabutterflies across Europe

Patterns of host use by brood parasiticMaculineabutterflies across Europe

Low Host Specialization in the Cuckoo Wasp, Parnopes grandior, Weakens Chemical Mimicry but Does Not Lead to Local Adaption

Evidence of a fixed polymorphism of one‐year and two‐year larval growth in the myrmecophilous butterfly Maculinea rebeli

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