In:
Proceedings of the National Academy of Sciences, Proceedings of the National Academy of Sciences, Vol. 109, No. 8 ( 2012-02-21)
Abstract:
The Parcoblatta species complex, consisting of 12 species endemic to North America, constitutes excellent material for future studies of premating reproductive isolation. The compound we isolated from P. lata attracted males of some other Parcoblatta species but not others. This observation suggests that Parcoblatta species likely use species-specific multicomponent pheromone blends, as do many other insects. Some species that were not attracted to parcoblattalactone may have greater fidelity to their multicomponent pheromone blend, or they may use a different major component, not parcoblattalactone, in their pheromone blend. Interestingly, however, P. virginica and P. caudelli males also were attracted to volatile emissions of P. lata females that contained the full blend of pheromone components. This unusual observation suggests that other species-isolating mechanisms may operate in this genus, such as temporal and spatial partitioning of sexual activity of different species within the forest. Parcoblatta females also may use species-specific contact sex pheromones to elicit courtship only from conspecific males. These results show that parcoblattalactone can attract not only P. lata but also several other Parcoblatta species, emphasizing its utility in monitoring several endemic wood cockroach species in red-cockaded woodpecker habitats. This macrocyclic lactone is a previously unidentified natural product and a previously unknown pheromonal structure for cockroaches, highlighting the great chemical diversity that characterizes olfactory communication in cockroaches—each long-range sex pheromone identified to date from different genera belongs to a different chemical class. As innovative natural product chemists, cockroaches have undergone adaptive radiations in their sexual communication signals, producing highly diverse and often unique sexual attractants and consequently fashioning relatively “private” channels of olfactory communication ( 5 ). The male cockroach, however, is the best judge whether we successfully deciphered its sexual communication code. We first tested the synthetic parcoblattalactone by monitoring the electrophysiological responses of isolated antennae of adult male P. lata , Parcoblatta virginica , and Parcoblatta pennsylvanica that were freshly collected in the same pine forest in Raleigh, NC. Both P. lata and P. virginica responded to as little as ∼0.1 ng of the pheromone, but P. pennsylvanica antennae responded only to very large amounts of parcoblattalactone. These results were confirmed with traps baited with parcoblattalactone that we deployed overnight in a mixed pine-hardwood forest in Raleigh. Sticky traps baited with 10, 100, and 1,000 ng parcoblattalactone attracted large numbers of adult males of four Parcoblatta species, most commonly P. lata , P. virginica , and P. caudelli , but not a single P. pennsylvanica , even though that species was clearly found in this forest ( Fig. P1 ). No immature Parcoblatta were found on any of the traps; one or two adult females were trapped in some traps but were found equally in baited and unbaited traps. Our previous analysis showed that the sex pheromone is produced in the anterior seven segments of sexually mature virgin females ( 2 ). We extracted 1,400 virgin females in hexane, and, while separating the extract by gas chromatography (GC), we also coupled the effluent of the GC to an isolated male antenna, which was used as a biological detector (electroantennographic detection; GC-EAD) ( 3 ). Sensilla on the male antennae house highly specialized receptors that are exquisitely sensitive to the female pheromone. GC-EAD analyses revealed four electrophysiologically active compounds. We concentrated on the most abundant compound, which also stimulated strong behavioral responses (upwind running and correct choice in a two-choice maze) from males. Analysis by GC coupled to a mass spectrometer (GC-MS) showed that this compound did not match any of the hundreds of thousands of compounds in the MS library. Although it gave us important clues as to the molecular formula and its molecular weight, MS was not sufficient to decipher the full chemical structure. Likewise, infrared spectroscopy coupled to the GC yielded some more clues but not the full structure. To obtain a tiny amount of absolutely pure pheromone for highly sensitive NMR experiments, we turned to a home-made preparative GC apparatus ( 4 ). In this procedure, each application of an extract into the GC column was followed by collection of the pheromone as it eluted out of the column. The procedure we developed allows the accumulation of successive trappings of the pheromone from multiple GC separations. Finally, the trap, containing less than 2 μg of the pheromone, was transferred directly into an NMR microcapillary tube, using only about 7 μL of solvent. This sample was flown immediately from North Carolina State University to the State University of New York in Syracuse, NY for hand-delivery directly to the NMR instrument. The spectra we obtained were remarkably clean and permitted us to propose the structure of the pheromone as (4 Z ,11 Z )-oxacyclotrideca-4,11-dien-2-one [synonym, (3 Z ,10 Z )-dodecadienolide], which we named “parcoblattalactone” because of its origin from Parcoblatta and its macrocyclic lactone structure. This compound was synthesized and was confirmed unambiguously to be the same as the natural pheromone by comparing the two NMR spectra. Wood cockroaches in the genus Parcoblatta , comprising 12 species endemic to North America, are highly abundant in southeastern pine forests and represent an important prey of the endangered red-cockaded woodpecker, Picoides borealis . The broad wood cockroach, Parcoblatta lata , is among the largest and most abundant of the wood cockroaches, constituting 〉 50% of the biomass of the woodpecker's diet ( 1 ). Because reproduction in red-cockaded woodpeckers is affected dramatically by seasonal and spatial changes in arthropod prey availability, monitoring P. lata populations could serve as a useful index of habitat suitability for woodpecker conservation and forest management efforts. Current efforts to assess habitat quality and prey availability entail exceptional investment in broad-scale monitoring with nonselective traps such as burlap bands on trees or cardboard, pitfall, and light traps. A synthetic sex pheromone of P. lata , a major prey, holds promise as an important economically and ecologically sound tool to monitor the quality and suitability of foraging habitats for red-cockaded woodpeckers. We describe here the identification, synthesis, and confirmation of the chemical structure of this pheromone.
Type of Medium:
Online Resource
ISSN:
0027-8424
,
1091-6490
DOI:
10.1073/pnas.1111748109
Language:
English
Publisher:
Proceedings of the National Academy of Sciences
Publication Date:
2012
detail.hit.zdb_id:
209104-5
detail.hit.zdb_id:
1461794-8
SSG:
11
SSG:
12
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