Early Quality Assessment Lessens Pheromone Specificity in a Moth
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Early quality assessment lessens pheromone specificity in a moth Zsolt Kárpátia, Marco Tasinb, Ring T. Cardéc, and Teun Dekkerd,1 aDepartment of Zoology, Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, H-1525, Budapest, Hungary; bUnit of Integrated Plant Protection and dUnit of Chemical Ecology, Swedish University of Agricultural Sciences, SE-230 53 Alnarp, Sweden; and cDepartment of Entomology, University of California, Riverside, CA 92521 Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved March 27, 2013 (received for review October 4, 2012) Pheromone orientation in moths is an exemplar of olfactory from activation, wing fanning, taking flight, locking onto the acuity. To avoid heterospecific mating, males respond to female- plume, and landing (7). An emergent property of studies on moth produced blends with high specificity and temporal resolution. A pheromone orientation is that blend ratios are equally important finely tuned sensory to projection neuron network secures spec- from activation to source finding (7). In line with this, it is thought ificity, and this network is thought to assess pheromone quality that males continuously assess quality during reiterative encounters continually during orientation. We tested whether male moths do with pheromone filaments in spatiotemporally dynamic plumes. indeed evaluate each pheromone encounter and surprisingly The crambid moth Ostrinia nubilalis is a species well known found that male European corn borer moths instead generalize for its narrow tuning to a binary blend of female produced (Z)- across successive encounters. Although initially highly ratio spe- 11-tetradecenyl acetate (Z11) and (E)-11-tetradecenyl acetate cific, once “locked on” to the pheromone plume the acceptable (E11) (8, 9). Two strains exist, the Z and E strains, which pro- ratio can vary widely, and even unattractive blends can become duce and prefer opposite ratios of Z11 and E11, 97:3 and 1:99 attractive. We further found that this “mental shortcut” may be Z11:E11, respectively. This has made this species a model for a consequence of the fact that sensory neurons exposed to fre- neurophysiological and evolutionary studies on blend production quent encounters do not reliably encode blend ratios. Neurons and preference (5, 6, 10). However, despite the reportedly high tuned to either of the two pheromone components adapt differ- pheromone specificity of males, strains interbreed in the field, as entially in plumes containing the preferred blend ratio (97:3) and sympatric populations may consist of up to 15% of hybrids (11, EVOLUTION cause the olfactory sensory signal to “evolve,” even in narrowly 12). Here, we investigate how pheromone communication, an tuned pheromonal circuits. However, apparently the brain inter- exemplar of olfactory specificity, may break down and mitigate prets these shifting signals as invariant “gestalts.” Generalization purifying selection. Implications for our understanding of olfac- in pheromone perception may mitigate stabilizing selection and tory coding and preference in general are also considered. allow introgression between sympatric strains, such as in the Eu- ropean corn borer, that otherwise appear isolated by pheromonal Results and Discussion differences. Generalization may also be important in responses to In a laminar flow wind tunnel (Fig. 1), we confirmed that Z males general odorants, as circuits underlying these display vast sensi- are highly specific to their own pheromone. Nearly 100% of the tivity differences, complex interactions, and temporal intricacies. Z males flew to a source of their own blend (Fig. 2A), only 10% flew to the intermediate blend [hybrid (H) blend, 50:50 Z11: blend recognition | odor processing | sensory constraints | evolution | E11], and the E lure did not induce any upwind flight (30-μg sexual selection septum load, Kruskal–Wallis rank test, P = 0.021). This supports wind tunnel studies that show that O. nubilalis males are attracted n moths, pheromones dominate mate finding. Female-produced to ratios close to those produced by females of their own strain (9). Ipheromones generally consist of a blend of two to several long- Thus, where both strains are sympatric, cross-strain attraction chain derivatives of fatty acids. The composition and ratio of and hybridization should be very rare for such narrowly tuned these components create species-specific blends, and males are species. Surprisingly, however, in the field, rates of hybridization, narrowly tuned to these to reduce the chance of heterospecific which produces viable individuals with intermediate pheromone – matings. Because of its high specificity, moth pheromone com- production and preference (8), can be as high as 15% (11 13). fi munication has been important in understanding species recog- This is hard to explain on the basis of the high speci city dem- nition and the evolutionary processes underlying signal evolution onstrated in numerous wind tunnel studies, including ours. We fi (1). In addition, owing to its simplicity, moth pheromone commu- hypothesized that, in the eld, close proximity of calling females of different strains might cause pheromone plumes to overlap nication has been a prime model for odor-mediated behavior, as fi well as olfactory detection, processing, and blend recognition (2–6). and lower through some mechanism the speci city of males. To test this, we exposed males in a laminar flow wind tunnel (Fig. In the current models, male moths respond to successive encounters 1A) to partially overlapping pheromone plumes, such as could of pheromone filaments within a plume by surging upwind. Flights occur in nature at high population densities. In a choice between slowly revert to casting (flying across the wind line without upwind three partially overlapping pheromone sources (Z blend, H progress) if sufficient time (generally less than a second) has passed “ ” blend, and E blend; Fig. 2B), Z males indeed lowered their since the last contact with such whiffs of pheromone (3, 4). specificity, with 58%, 38%, and 4% of the males landing on Z, H, Moths are exquisitely sensitive to the odor plume’s fine-scale structure (3, 4) and can resolve the composition of a blend on a millisecond timescale, both behaviorally and physiologically. Author contributions: Z.K., M.T., R.T.C., and T.D. designed research; Z.K., M.T., and T.D. Male Heliothis virescens perceived pheromone and antagonist as performed research; Z.K., M.T., R.T.C., and T.D. analyzed data; and R.T.C. and T.D. wrote “separate” if strands were encountered only 1 ms apart (2). the paper. Similarly, only simultaneous arrival of pheromone components The authors declare no conflict of interest. triggered the response of blend-sensitive projection neurons in This article is a PNAS Direct Submission. the brain (4). Furthermore, the complete blend has been viewed 1To whom correspondence should be addressed. E-mail: [email protected]. as dictating all responses from activation to mating, with the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. natural ratio having the lowest threshold for inducing all behaviors, 1073/pnas.1216145110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1216145110 PNAS Early Edition | 1of6 Downloaded by guest on September 29, 2021 and E lures, respectively (Fig. 2B, χ2 test, P = 0.0069, n = 90). led light The position of the lures (left–center–right: Z–H–E, E–Z–H, or H–E–Z) had no significant effect (χ2 = 7.32, df = 4, P = 0.12). video After taking flight, males apparently relax their specificity. camera The decrease in specificity likely occurs once a male engages in sustained upwind flight (locks onto the plume). To test this, we created plumes that transitioned seamlessly from one blend into A another (see sample tracks; Fig. 1B). Once a male locked onto the plume, sources were swapped. All Z males casted as soon as wind fl 70 cm they ew from a Z-blend plume into clean air, which shows that filaments of Z-blend pheromone did not linger in the wind tunnel after the swap (Fig. 2C). In contrast, male moths continued up- wind without interruption when blends were swapped from a Z blend to a Z blend, as also shown by their track angles (Fig. 2D). 70 cm How did switching to a new blend affect upwind flight? Sur- prisingly, flights were undisturbed by a swap from the Z blend to the H blend (Figs. 2C and 1B). In fact, the track angle and source finding rates were indistinguishable to the Z-blend swap (Fig. 200 cm LED light stimulus 2D). Moreover, when Z males commenced in the Z blend, but controller contorller entered an E-blend plume, 52% continued upwind, with 28% of these males landing on the source of the E blend. The remaining B 48% of the males ceased upwind flight (Fig. 2C). This is also swap Z to clean air downwind upwind reflected in the track angle. After transiting into clean air, moth 200 cm projected their flights more crosswind. However, the average track angles did not change after swapping to the Z blend or to the H blend (one-way ANOVA, P = 0.48 and 0.35, respectively). release tube Although swapping from the Z blend to the E blend increased sources the moth’s average track angle (from 61° to 74°, P < 0.0001), it 70 cm was subsequently kept constant over time, resulting in a signifi- cant portion of source finding. These findings are remarkable, as in one-choice trials the H blend induced orientation in only 10% of the males, whereas the E blend never induced any response swap Z to Z (Fig. 2A). This demonstrates that, once males have locked onto the plume, they are substantially less attuned to blend quality, which likely explains the occurrence of hybrids in nature. “Lock- ing onto the plume” as a decisive step in moth orientation is also implied in other studies (e.g., refs.