Deceptive signals and behaviors of a cleptoparasitic beetle show local adaptation to different host bee species

Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved August 2, 2018 (received for review October 26, 2017)
September 10, 2018
115 (39) 9756-9760

Significance

This study provides strong evidence for two different but complementary types of local adaptation in geographically isolated populations of a parasitic insect. Specifically, we report that different populations of a blister beetle, Meloe franciscanus, a nest parasite of bees, locally adapt their deceptive chemical signals, which mimic the sex pheromones of their host bees, to the differing pheromone blends of their local host species. We show that local nest parasites are significantly more attractive to male bees than nonlocal parasites, using transplant experiments. We report the identification of attractant blends for the two host species and the compounds that the beetle larvae produce to attract their hosts. Furthermore, we show that the two parasite populations have evolved divergent host-matching behaviors.

Abstract

Chemosensory signals play a key role in species recognition and mate location in both invertebrate and vertebrate species. Closely related species often produce similar but distinct signals by varying the ratios or components in pheromone blends to avoid interference in their communication channels and minimize cross-attraction among congeners. However, exploitation of reproductive signals by predators and parasites also may provide strong selective pressure on signal phenotypes. For example, bolas spiders mimic the pheromones of several moth species to attract their prey, and parasitic blister beetle larvae, known as triungulins, cooperatively produce an olfactory signal that mimics the sex pheromone of their female host bees to attract male bees, as the first step in being transported by their hosts to their nests. In both cases, there is strong selection pressure on the host to discriminate real mates from aggressive mimics and, conversely, on the predator, parasite, or parasitoid to track and locally adapt to the evolving signals of its hosts. Here we show local adaptation of a beetle, Meloe franciscanus (Coleoptera: Meloidae), to the pheromone chemistry and mate location behavior of its hosts, two species of solitary bees in the genus Habropoda. We report that M. franciscanus’ deceptive signal is locally host-adapted in its chemical composition and ratio of components, with host bees from each allopatric population preferring the deceptive signals of their sympatric parasite population. Furthermore, in different locales, the triungulin aggregations have adapted their perching height to the height at which local male bees typically patrol for females.
Species recognition and mate location chemosensory signals play key roles in both invertebrate and vertebrate species (1, 2). Predators such as bolas spiders, parasites (3), and parasitoids such as blister beetle larvae (4) can exploit these communication signals. Parasites are expected to exhibit local adaptations to their host populations because, in general, parasites exhibit larger population sizes and shorter generation times than their hosts (5, 6) (but also see ref. 7). The beetle Meloe franciscanus (Coleoptera: Meloidae), the larvae of which parasitize ground-nesting bees, has neither of these stereotypical characteristics. First, M. franciscanus is univoltine, with a similar generation time as its host, and second, its population sizes are small relative to those of its hosts. The adult beetles are flightless and have limited capacity to disperse (8), but beetles can disperse phoretically as larvae attached to host bees (9). In addition, the various extant populations of M. franciscanus are geographically isolated, with minimal or no possibility of gene flow between populations. Here we report that different populations of M. franciscanus exhibit local adaptations that mimic both the behaviors and the chemical composition of the sex pheromones of locally available bee species. Specifically, we compare a population of M. franciscanus larvae, known as triungulins, parasitizing nests of Habropoda miserabilis (Hymenoptera: Apidae) from the coastal sand dunes of Oregon with a population parasitizing the congener Habropoda pallida in the Mojave Desert in south-central California. It must be emphasized that these M. franciscanus populations have been determined to be the same species using both morphological (10) and molecular analyses (11).
Female M. franciscanus lay large egg masses averaging 761 eggs (SD 533, n = 8) (4). The eggs hatch synchronously, and the newly hatched triungulins climb nearby vegetation to form a single aggregation (4, 12). These aggregations remain together for up to 14 d, during which time they produce a signal that mimics the sex pheromone produced by females of their bee hosts (4, 12). It is essential that they act collectively to produce a signal of sufficient intensity. Their olfactory signal attracts male bees to pseudocopulate, and the instant that a male bee contacts an aggregation, the entire larval mass attaches to the male (Fig. 1). The male then flies off with his unwanted passengers, which transfer to a female during mating or mating attempts (4). The infested female then carries the triungulins to their ultimate destination, the female bee’s nest, where they disembark to feed on the nest provisions and host offspring, completing their development and emerging from the nest as adults the following spring (8, 9).
Fig. 1.
Cleptoparasite M. franciscanus adapts to two allopatric bee hosts in the genus Habropoda. (A) A male H. 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) An M. 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 pheromone of female H. pallida was produced in the head, and consists of a group of odd-numbered, C21-to-C31 monounsaturated hydrocarbons (4). Of these components, those with double bonds at the 9 position were found from both males and females, whereas only females produced alkenes with double bonds in positions other than 9, and it was these additional isomers that made the signal sex-specific. We also showed that the triungulins parasitizing this population mimicked a subset of the female-specific alkenes, with the subset being both necessary and sufficient to attract male bees effectively.
A recent meta-analysis of hymenopteran sex pheromones suggests that both saturated and unsaturated hydrocarbons are strongly correlated with evolutionary relationships within the order, and alkenes with a (Z)-9 double bond were suggested as the ancestral state (13). Divergence from the ancestral state has resulted in double bonds in other positions, greatly increasing the number of different signals possible, particularly as compounds can occur as blends. Selection favors receivers’ ability to detect divergent ratios or components (14), providing a mechanism by which signals can evolve in response to selection pressures such as interspecific competition for a pheromone channel or exploitation of the signal by predators and parasites. Over time, as populations become isolated in space and/or time, the different localized forces of natural selection result in divergence of the signals from the ancestral state. Furthermore, in systems where parasites or predators exploit the signals of their hosts, exploiting organisms must track the evolving signals of their local hosts or multiple hosts to persist. Here we provide evidence for local adaptation by M. franciscanus, demonstrating how populations have matched both the pheromone chemistry and the reproductive behaviors of their local hosts, two solitary bee species in the genus Habropoda.

Results

Cafeteria Experiments.

In a first set of experiments, we showed that H. miserabilis females from Oregon produced a sex pheromone that attracted males, and that aggregations of sympatric M. franciscanus larvae also attracted male bees. Thus, male bees were highly attracted to cages containing live female bees, but not to caged live male bees or to control, empty cages (Fig. 2A and SI Appendix, Table S2). Furthermore, male bees were attracted to caged aggregations of M. franciscanus triungulins, suggesting that they too produced a volatile attractant. A follow-up experiment testing different body parts (female and male bee head, thorax, abdomen) showed that males were most attracted to the heads of females (Fig. 2B and SI Appendix, Table S3). Body parts of males were not attractive (SI Appendix, Table S3), demonstrating the sexual specificity of the signal. We then analyzed extracts of heads of H. miserabilis bees of both sexes and whole-body extracts of sympatric triungulin aggregations. A subset of compounds found in the extracts of the triungulins was also found in extracts of the heads of female H. miserabilis bees. The extracts consisted almost exclusively of straight-chain alkanes and alkenes. The extract of heads of male bees was the least complex, consisting primarily of tricosane (C23) and pentacosane (C25) and three alkenes with (Z)-9 double bonds [(Z)-9-C23, (Z)-9-C25, and (Z)-9-C31], with (Z)-9-C25 being the most abundant (Fig. 3). In contrast, extracts of the heads of female bees were characterized by 5 alkanes with chain lengths of C21 to C29 and 12 alkenes with chain lengths of C23 to C29 and with double bonds in positions 7, 10, 11, 12, 13, and 14 but not position 9 (Fig. 3). The whole-body extracts of the triungulins were intermediate, with 5 alkanes between C21 and C29 and 8 alkenes with double bonds in positions 7, 9, 10, 11, and 12 (Fig. 3).
Fig. 2.
(A) Male H. miserabilis were significantly more attracted to caged female bees and M. franciscanus larval aggregations than to caged male bees (Friedman test: χ2 = 20.52, P < 0.001, k = 4, n = 9). Female bees were significantly more attractive than male bees (P = 0.014). Female bee and Meloe aggregation attraction were not significantly different from each other (P = 0.998), and both were significantly more attractive than controls (females, P = 0.014; Meloe aggregations, P = 0.024). However, male bees were not significantly different from controls (P = 1.00) (SI Appendix, Table S2). (B) Body regions of the two sexes differed in attractiveness (Friedman test: F = 4.55, χ2 = 42.98, k = 9, P < 0.001, n = 7). Female bee heads were significantly more attractive to male bees than female thoraxes, all male body segments, and controls (P = 0.001). Male body regions did not differ significantly from controls (P = 1.00; male thorax, P = 0.879) (male data are in SI Appendix, Table S3). (C) Synthetic lures (syn lure OR) reconstructed from analyses of local Oregon M. franciscanus triungulins were more attractive to male H. miserabilis bees than were control lures (Poisson GLIMMIX trial: F = 4.31, df = 3, P = 0.131; treatment: F = 24.58, df = 1, P = 0.016; n = 4, control 0 ± 0.0 SEM) (SI Appendix, Table S4). Figures show means ± SEM of male inspections and contacts of test subjects in cafeteria experiments. Blue bars represent bees or bee body parts; gold bars represent Meloe larval aggregations or Meloe syn lure. The different lowercase letters in AC indicate that the inspections + contacts were significantly different from each other.
Fig. 3.
M. franciscanus triungulins from different populations produce locally adapted blends of semiochemicals to mimic their specific host bees. Chemical profiles of (A) the Oregon population of host bee H. miserabilis and its locally adapted nest parasite M. franciscanus, and (B) the Mojave Desert population of host bee H. pallida and its locally adapted nest parasite M. franciscanus. Bars in blue are alkenes, which are present in the extracts of female and male bees and/or locally adapted triungulins. Note the presence of (Z)-7-C23 in female H. miserabilis and Oregon M. franciscanus. The blue-shaded sections highlight the areas of mimicry between local M. franciscanus and Habropoda females and the area of difference between the two Meloe populations and the two Habropoda species. The asterisk indicates the most abundant compound differed between extracts. [B is reprinted with permission from ref. 4. Copyright (2006) National Academy of Sciences, USA.]
In comparing the chemistries of the H. miserabilis bees and triungulins from the cool Oregon site and the previously studied H. pallida bees from the Mojave Desert site, the extracts were superficially similar, consisting of complex mixtures of alkanes and alkenes. However, closer examination revealed major differences. For example, the Oregon H. miserabilis females had three (Z)-7-alkenes [(Z)-7-C23, (Z)-7-C25, and (Z)-7-C27] that were absent in the H. pallida Mojave females. Conversely, H. pallida Mojave females had three (Z)-9-alkenes [(Z)-9-C21, (Z)-9-C23, and (Z)-9-C25] that were absent in H. miserabilis Oregon females, as well as a group of higher molecular mass C31 alkenes. The triungulin extracts from the two sites were also markedly different. The triungulins from both sites had (Z)-9-C23 and (Z)-9-C25, whereas only the Oregon triungulins had (Z)-7-C23 and (Z)-7-C25, each matching local host female bees. The proportions of the individual alkenes in the beetle extracts also differed between the Mojave and Oregon populations.
Finally, a blend of compounds found in extracts of both the female H. miserabilis bees and the Oregon triungulins, reconstructed from synthetic compounds, was attractive to male H. miserabilis in a field bioassay (Fig. 2C and SI Appendix, Table S4), confirming that the Oregon triungulins have adapted their mimicry of their host’s sex pheromone to the local host species. We had previously documented the attraction of Mojave male H. pallida to the synthetic blend of Mojave M. franciscanus triungulins (4).

Transplant Experiments.

To determine whether the triungulin populations parasitizing the different allopatric bee species have locally adapted to the chemical signals of their respective hosts, we tested responses of male bees to sympatric and allopatric triungulin aggregations. We found that male bees were significantly more attracted to triungulin aggregations from their own locale than to allopatric aggregations, for both bee species (Fig. 4 and SI Appendix, Table S5), confirming the parasites’ ability to track the pheromones of their coevolved hosts.
Fig. 4.
Reciprocal transplant experiments showed that male Habropoda bees were most attracted to their local M. franciscanus triungulin aggregations. M. franciscanus larval aggregations transplanted from the Mojave Desert to the Oregon site were significantly less attractive to male H. miserabilis than were local M. franciscanus aggregations from Oregon (GLmixedM: P < 0.0006, n = 5). Similarly, M. franciscanus larval aggregations transplanted from Oregon to the Mojave Desert study site were less attractive to male H. pallida bees than local Mojave M. franciscanus aggregations (GLmixedM: P < 0.001, n = 3) (SI Appendix, Table S5). Figures show means ± SEM of male inspections and contacts of test subjects in cafeteria experiments.

Behavioral Adaptation.

We observed that H. miserabilis males at the Oregon sand dunes site typically flew 2 to 12 cm above the ground while patrolling for emerging females, whereas H. pallida males in the Mojave Desert flew 10 to 40 cm above the ground while patrolling for emerging females. Consequently, we tested whether the two populations of triungulins varied in their preferred aggregation heights. We found that Oregon triungulins aggregated at a significantly lower height in their native Oregon range (n = 53) and maintained this height when transplanted as egg masses and allowed to emerge at the Mojave Desert site (Fig. 5 and SI Appendix, Fig. S1 and Table S6). Similarly, Mojave triungulin aggregations (n = 53) studied in the Mojave Desert showed an innate preference for significantly higher aggregation heights than Oregon triungulins, even when transplanted as egg masses to the Oregon site (n = 23) (Fig. 5). Thus, local stimuli are not needed to elicit this response (15), and selection of high or low aggregation sites is not due to the heights of available perches or temperature. Instead, perching height appears to be genetically determined, as an adaptation to the heights at which local male bees typically patrol (SI Appendix, Fig. S1).
Fig. 5.
Triungulin aggregations show local adaptation in perching heights. The aggregation heights of M. franciscanus larvae from the Mojave Desert (34.94 ± 2.35 cm SEM) and tested in the Mojave Desert and in the Oregon coastal sand dunes were not significantly different (gold bars). Similarly, the aggregation heights of M. franciscanus from coastal Oregon (8.07 ± 0.70 cm SEM) and tested in the Mojave Desert and in coastal sand dunes in Oregon were not significantly different (blue bars). The aggregation heights of the Mojave Desert and the Oregon populations are significantly different at both sites (Kruskal–Wallis: P < 0.001, n = 53) (SI Appendix, Table S6). The different lowercase letters (a and b) indicate that the perching heights of the Meloe larvae from different populations (Mojave, OR) were significantly different from each other when tested in different locations (transplant experiments).

Discussion

We identified two separate but complementary local adaptations by two geographically isolated populations of a cleptoparasitic species, which allow these parasites to exploit two different host species in different parts of their range. Our reciprocal transplant experiments confirmed that these traits reflect innate genetic differences, rather than phenotypic plasticity, in response to differences in environmental conditions between coastal sand dunes in Oregon and California’s Mojave Desert. Further studies are needed to investigate the selection pressures that the parasites exert on the chemical signaling and reproductive behaviors of their hosts and, in turn, the reciprocal selection on the parasites themselves. Understanding the evolutionary forces that shape local adaptation is fundamental to understanding parasite speciation and the maintenance of enduring parasite–host relationships.

Methods

Collection of Insects and Field Experiments.

Specimens were collected from and field bioassays were conducted at Hidden Lake Dunes north of Waldport, Lincoln County, Oregon (N44.45666667, W-124.0794444, 14 m) and Kelso Dunes in the Mojave National Preserve, San Bernardino County, California (N34.88968, W-115.72147, 760 m), from March through May 2010 to 2015. Sand dunes at the Oregon site are stabilized with European beach grass, Ammophila arenaria (L.) Link, surrounded by Scotch broom Cystisus scoparius (L.) Link. A forest composed of Pinus contorta Douglas ex Loudon var. contorta and California huckleberry Vaccinium ovatum Pursh, the local major host plant of adult H. miserabilis, surrounds the nest site. Kelso Dunes are active dunes which support ∼184 species of plants (16), including Astragalus lentiginosus var. borreganus, a nectar plant of H. pallida and the exclusive host plant of adult M. franciscanus at Kelso Dunes; Larrea tridentata, which is the major pollen host plant of H. pallida; Petalonyx thurberi; and several native grasses including Hilaria rigida, Panicum urvilleanum, and Stipa hymenoides, which serve as triungulin aggregation perching sites. Astragalus l. var. borreganus blooms every year, providing a reliable nectar source for H. pallida, which emerges in synchrony with its bloom at Kelso Dunes. H. pallida nesting begins a few days after the onset of Larrea bloom.
Voucher specimens of M. franciscanus and host bees H. miserabilis and H. pallida from the multiple study localities in Oregon and California have been deposited in the Bohart Museum, University of California, Davis. Our sequence data for M. franciscanus, for the CO1, 16S, 28S, ITS-2, and EF1-α genes, are available in GenBank (SI Appendix, Table S1). The data from the experiments are provided in SI Appendix, Tables S2–S6.
To test for local adaptation, we conducted transplant experiments in two habitats (Mojave and Oregon) with local and transplanted Meloe aggregations, and used the trait male bee attraction as a measure of parasite performance (17). Cafeteria and transplant experiments conducted in the Oregon coastal dunes were performed from 10:00 to 17:00 hours during February through April 2010 to 2015. For the experiments testing perching heights, triungulins were released in the bottom of a vial containing a vertical 60-cm-long wooden dowel, and allowed to climb to their preferred height inside a screen cage. Each cafeteria experiment presented all test subjects simultaneously within each trial, along with a control. After each trial was performed, positions of test treatments were randomly changed for each subsequent trial.
For bioassays of attractants, lures consisted of 11-mm gray rubber serum stoppers (The West Company) or 1-cm squares of dark brown felt cloth treated with hexane extracts of heads, thoraxes, and abdomens of male and female H. pallida or H. miserabilis or local M. franciscanus triungulins, or hexane solutions of test compounds (typical dose 0.5 mg of the major component, with amounts of the minor components corresponding to ratios found in the extracts). Controls consisted of identical materials (stoppers, felt cloth, cages, pins, or wood dowels) treated with hexane rather than extracts or compounds. Bioassays tested attraction to (i) live bees or triungulins in cages, versus empty cage controls; (ii) attraction to bee body parts, versus controls; and (iii) triungulin aggregations from Oregon, versus triungulin aggregations from Kelso Dunes. At Kelso Dunes, lures, controls (hexane-treated septa or empty screen cubes), and cages were placed at ∼60-cm height above the sand surface on the dowels within the Meloe aggregation height range in patches of plants located in dune depressions that were regularly visited by bees of both sexes. At the Oregon coastal dunes site, lures, controls, or cages were placed on insect pins on the ground. For all bioassays, the number of male bee inspection hovers and contacts to cages containing live bees or triungulins, lures, or controls, and the behaviors of bees around the various treatments, were recorded by visual observations. These behaviors were defined as male bees approaching females, triungulin aggregations, a lure, or cage, within 10 cm for ≥2 s (11, 18). The bees are sexually dimorphic, so sex of responding animals could be determined visually at close range. Real-time notes were used for analysis. Subsets of responding animals were caught with a sweep net to verify that they were males, and bioassays were recorded by digital video as vouchers. Heights of natural aggregations were measured at both study sites. Air temperature and wind speed for each experiment were recorded with a Kestrel 4500 anemometer.

Chemical Analysis.

Individual male and female H. pallida and H. miserabilis bees were collected with a sweep net and held in glass vials. After brief chilling, each bee was dissected into head, thorax, and abdomen, and each body part was extracted with 1 mL hexane for 1 h. Triungulin aggregations were extracted in 1 mL hexane for 1 h. The resulting extracts from bee body parts or triungulins were transferred to clean vials for use in bioassays, or stored at −20 °C until analyzed by coupled gas chromatography–mass spectrometry (GC-MS).
Extracts of triungulin aggregations, and of heads, thoraxes, and abdomens of male and female H. miserabilis, were analyzed by GC-MS, using a Hewlett-Packard 6890 gas chromatograph interfaced to an HP 5973 mass selective detector (Hewlett-Packard) operated in electron impact ionization mode (70 eV). The gas chromatograph was equipped with a DB-5MS column (20 m × 0.2 mm i.d., 0.25-μm film thickness; J&W Scientific), with helium carrier gas with a flow rate of 37 cm/s, injector and transfer line temperatures of 280 °C, and a temperature program of 100 °C/0 min, 15 °C/min to 280 °C, hold time 30 min. Sample aliquots (1 μL) were injected in splitless mode.
To determine the positions and stereochemistries of the alkene double bonds, 100-μL aliquots of extracts were concentrated to dryness under a stream of nitrogen and treated with five drops of a solution of meta-chloroperbenzoic acid in methylene chloride (2 mg/mL) for 2 h at room temperature. The solutions were concentrated to dryness and the residue was treated with 200 μL 1 M aqueous NaOH and 0.5 mL hexane, and vortexed. The hexane layer was removed and dried by passage through a plug of anhydrous Na2SO4 in a pipette, concentrated, and analyzed by GC-MS. The positions of the derivatized double bonds were determined from the enhanced fragments from cleavage on either side of the epoxide, and the geometries of the former double bonds were determined by epoxidation of authentic standards and matching of retention times. Epoxides from the (Z)- and (E)-alkenes separated to baseline, with the (E)-isomers eluting first. Straight-chain alkanes were obtained from commercial sources. (Z)-9-heneicosene and (Z)-9-tricosene were purchased from Sigma Chemical and Lancaster Synthesis, respectively. Other (Z)-alkenes were synthesized by (Z)-selective Wittig reactions, and purified by recrystallization as previously described (19). The synthetic reconstruction of compounds identified in extracts of the Oregon triungulins and the H. miserabilis females consisted of tricosane (0.5 mg), (Z)-7-tricosene (0.5 mg), (Z)-9-tricosene (1 mg), and (Z)-11-tricosene (0.5 mg), loaded onto gray rubber septa as a hexane solution.

Statistical Analysis.

To analyze our transplant experiments, we used R (20) and lme4 (21) to perform a linear mixed effects analysis of the relationship between the mean inspections and contacts of male bees to the local versus transplanted Meloe aggregations. The random effects specified were trial location and type of aggregation (origin) [glm(formula = meanIC ∼ trialloc + type, family = poisson, data = choice.dat)]. To analyze our cafeteria experiments with live bees and Meloe aggregations, as well as female and male bee heads, abdomens, and thoraxes, we used the Friedman test (two-way nonparametric ANOVA) followed by a posteriori multiple comparisons using the Nemenyi multiple comparison test for unreplicated blocked data with the PMCMR package (version 4.0.0, 2018) in R (22). The synthetic lure experiments were analyzed with a Poisson GLIMMIX procedure in SAS (23). The P values for the Friedman tests used to analyze Habropoda and Meloe aggregation and different body part attractiveness to male H. miserabilis bees were derived from tables (24).

Data Availability

Data deposition: The sequences reported in this paper have been deposited in GenBank database (accession nos. MH487729.1–MH487733.1, MH489082.1–MH489086.1, MH491842.1–MH491845.1, MH511214.1–MH511218.1, and MH511209.1–MH511213.1) and are available in SI Appendix, Table S1. Experimental data are available in SI Appendix, Tables S1–S6.

Acknowledgments

We thank the following for their generous support of this research: The Community Foundation’s Desert Legacy Fund, California Desert Research, Disney Wildlife Conservation Fund, Sean and Anne Duffey and Hugh and Geraldine Dingle Research Fellowship, and Department of Entomology and Nematology, University of California, Davis fellowships. We thank S. Nadler, J. Rosenheim, J. D. Pinto, R. Westcott, N. Gershenz, and C. Pagan and our reviewers for helpful suggestions and comments that greatly improved this manuscript.

Supporting Information

Appendix (PDF)

References

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 115 | No. 39
September 25, 2018
PubMed: 30201716

Classifications

Data Availability

Data deposition: The sequences reported in this paper have been deposited in GenBank database (accession nos. MH487729.1–MH487733.1, MH489082.1–MH489086.1, MH491842.1–MH491845.1, MH511214.1–MH511218.1, and MH511209.1–MH511213.1) and are available in SI Appendix, Table S1. Experimental data are available in SI Appendix, Tables S1–S6.

Submission history

Published online: September 10, 2018
Published in issue: September 25, 2018

Keywords

  1. local adaptation
  2. deceptive signals
  3. insect–parasite interactions
  4. behavioral adaptation
  5. mimicry

Acknowledgments

We thank the following for their generous support of this research: The Community Foundation’s Desert Legacy Fund, California Desert Research, Disney Wildlife Conservation Fund, Sean and Anne Duffey and Hugh and Geraldine Dingle Research Fellowship, and Department of Entomology and Nematology, University of California, Davis fellowships. We thank S. Nadler, J. Rosenheim, J. D. Pinto, R. Westcott, N. Gershenz, and C. Pagan and our reviewers for helpful suggestions and comments that greatly improved this manuscript.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Leslie Saul-Gershenz1 [email protected]
Department of Entomology and Nematology, University of California, Davis, CA 95616;
Jocelyn G. Millar
Department of Entomology, University of California, Riverside, CA 92521
J. Steven McElfresh
Department of Entomology, University of California, Riverside, CA 92521
Neal M. Williams
Department of Entomology and Nematology, University of California, Davis, CA 95616;

Notes

1
To whom correspondence should be addressed. Email: [email protected].
Author contributions: L.S.-G. and J.G.M. designed research; L.S.-G., J.G.M., and J.S.M. performed research; J.G.M. contributed new reagents/analytic tools; L.S.-G., J.G.M., J.S.M., and N.M.W. analyzed data; and L.S.-G., J.G.M., and N.M.W. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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