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Deceptive Signals and Behaviors of a Cleptoparasitic Beetle Show Local Adaptation to Different Host Bee Species

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Deceptive Signals and Behaviors of a Cleptoparasitic Beetle Show Local Adaptation to Different Host Bee Species Deceptive signals and behaviors of a cleptoparasitic beetle show local adaptation to different host bee species Leslie Saul-Gershenza,1, Jocelyn G. Millarb, J. Steven McElfreshb, and Neal M. Williamsa aDepartment of Entomology and Nematology, University of California, Davis, CA 95616; and bDepartment of Entomology, University of California, Riverside, CA 92521 Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved August 2, 2018 (received for review October 26, 2017) Chemosensory signals play a key role in species recognition and pallida in the Mojave Desert in south-central California. It must be mate location in both invertebrate and vertebrate species. Closely emphasized that these M. franciscanus populations have been related species often produce similar but distinct signals by determined to be the same species using both morphological (10) varying the ratios or components in pheromone blends to avoid and molecular analyses (11). interference in their communication channels and minimize cross- Female M. franciscanus lay large egg masses averaging 761 attraction among congeners. However, exploitation of reproduc- eggs (SD 533, n = 8) (4). The eggs hatch synchronously, and the tive signals by predators and parasites also may provide strong newly hatched triungulins climb nearby vegetation to form a selective pressure on signal phenotypes. For example, bolas single aggregation (4, 12). These aggregations remain together spiders mimic the pheromones of several moth species to attract their prey, and parasitic blister beetle larvae, known as triungulins, for up to 14 d, during which time they produce a signal that cooperatively produce an olfactory signal that mimics the sex mimics the sex pheromone produced by females of their bee pheromone of their female host bees to attract male bees, as the hosts (4, 12). It is essential that they act collectively to produce a first step in being transported by their hosts to their nests. In both signal of sufficient intensity. Their olfactory signal attracts male cases, there is strong selection pressure on the host to discriminate bees to pseudocopulate, and the instant that a male bee contacts EVOLUTION real mates from aggressive mimics and, conversely, on the predator, an aggregation, the entire larval mass attaches to the male (Fig. parasite, or parasitoid to track and locally adapt to the evolving 1). The male then flies off with his unwanted passengers, which signals of its hosts. Here we show local adaptation of a beetle, transfer to a female during mating or mating attempts (4). The Meloe franciscanus (Coleoptera: Meloidae), to the pheromone chem- infested female then carries the triungulins to their ultimate istry and mate location behavior of its hosts, two species of solitary destination, the female bee’s nest, where they disembark to feed bees in the genus Habropoda.WereportthatM. franciscanus’ de- on the nest provisions and host offspring, completing their de- ceptive signal is locally host-adapted in its chemical composition and ratio of components, with host bees from each allopatric population velopment and emerging from the nest as adults the following preferring the deceptive signals of their sympatric parasite popula- spring (8, 9). tion. Furthermore, in different locales, the triungulin aggregations have adapted their perching height to the height at which local Significance male bees typically patrol for females. This study provides strong evidence for two different but local adaptation | deceptive signals | insect–parasite interactions | complementary types of local adaptation in geographically behavioral adaptation | mimicry isolated populations of a parasitic insect. Specifically, we report that different populations of a blister beetle, Meloe francis- pecies recognition and mate location chemosensory signals canus, a nest parasite of bees, locally adapt their deceptive Splay key roles in both invertebrate and vertebrate species (1, chemical signals, which mimic the sex pheromones of their host 2). Predators such as bolas spiders, parasites (3), and parasitoids bees, to the differing pheromone blends of their local host such as blister beetle larvae (4) can exploit these communication species. We show that local nest parasites are significantly signals. Parasites are expected to exhibit local adaptations to more attractive to male bees than nonlocal parasites, using their host populations because, in general, parasites exhibit transplant experiments. We report the identification of at- larger population sizes and shorter generation times than their tractant blends for the two host species and the compounds hosts (5, 6) (but also see ref. 7). The beetle Meloe franciscanus that the beetle larvae produce to attract their hosts. Further- (Coleoptera: Meloidae), the larvae of which parasitize ground- more, we show that the two parasite populations have nesting bees, has neither of these stereotypical characteristics. evolved divergent host-matching behaviors. First, M. franciscanus is univoltine, with a similar generation time Author contributions: L.S.-G. and J.G.M. designed research; L.S.-G., J.G.M., and J.S.M. as its host, and second, its population sizes are small relative to performed research; J.G.M. contributed new reagents/analytic tools; L.S.-G., J.G.M., those of its hosts. The adult beetles are flightless and have lim- J.S.M., and N.M.W. analyzed data; and L.S.-G., J.G.M., and N.M.W. wrote the paper. ited capacity to disperse (8), but beetles can disperse phoretically The authors declare no conflict of interest. as larvae attached to host bees (9). In addition, the various extant This article is a PNAS Direct Submission. populations of M. franciscanus are geographically isolated, with Published under the PNAS license. minimal or no possibility of gene flow between populations. Here M. franciscanus Data deposition: The sequences reported in this paper have been deposited in GenBank we report that different populations of exhibit database (accession nos. MH487729.1–MH487733.1, MH489082.1–MH489086.1, MH491842.1– local adaptations that mimic both the behaviors and the chemical MH491845.1, MH511214.1–MH511218.1,andMH511209.1–MH511213.1) and are available in composition of the sex pheromones of locally available bee SI Appendix, Table S1. Experimental data are available in SI Appendix, Tables S1–S6. species. Specifically, we compare a population of M. franciscanus 1To whom correspondence should be addressed. Email: [email protected]. larvae, known as triungulins, parasitizing nests of Habropoda This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. miserabilis (Hymenoptera: Apidae) from the coastal sand dunes 1073/pnas.1718682115/-/DCSupplemental. of Oregon with a population parasitizing the congener Habropoda www.pnas.org/cgi/doi/10.1073/pnas.1718682115 PNAS Latest Articles | 1of5 Downloaded by guest on September 24, 2021 Fig. 1. Cleptoparasite M. franciscanus adapts to two allopatric bee hosts in the genus Habropoda.(A)AmaleH. pallida from the Mojave Desert with M. franciscanus triungulins attached. (B) A male H. miserabilis from Oregon with M. franciscanus triungulins covering the entire dorsal surface of the abdomen. (C)AnM. franciscanus aggregation on grass stems. [C is reprinted with permission from ref. 4. Copyright (2006) National Academy of Sciences, USA.] (All images, L.S.-G.) In a previous study, we showed that the sex attractant phero- populations become isolated in space and/or time, the different mone of female H. pallida was produced in the head, and consists localized forces of natural selection result in divergence of the of a group of odd-numbered, C21-to-C31 monounsaturated hy- signals from the ancestral state. Furthermore, in systems where drocarbons (4). Of these components, those with double bonds parasites or predators exploit the signals of their hosts, exploiting at the 9 position were found from both males and females, organisms must track the evolving signals of their local hosts or whereas only females produced alkenes with double bonds in multiple hosts to persist. Here we provide evidence for local positions other than 9, and it was these additional isomers that adaptation by M. franciscanus, demonstrating how populations made the signal sex-specific. We also showed that the triungulins have matched both the pheromone chemistry and the reproductive parasitizing this population mimicked a subset of the female- behaviors of their local hosts, two solitary bee species in the genus specific alkenes, with the subset being both necessary and suffi- Habropoda. cient to attract male bees effectively. A recent meta-analysis of hymenopteran sex pheromones Results suggests that both saturated and unsaturated hydrocarbons are Cafeteria Experiments. In a first set of experiments, we showed strongly correlated with evolutionary relationships within the that H. miserabilis females from Oregon produced a sex phero- order, and alkenes with a (Z)-9 double bond were suggested as mone that attracted males, and that aggregations of sympatric M. the ancestral state (13). Divergence from the ancestral state has franciscanus larvae also attracted male bees. Thus, male bees resulted in double bonds in other positions, greatly increasing the were highly attracted to cages containing live female bees, but number of different signals possible, particularly as compounds not to caged live male bees or to control, empty cages (Fig. 2A can occur as blends. Selection favors receivers’
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