The importance of insect behavior in Sterile Insect Technique (examples from the Diptera)

1. The importance of insect behavior in Sterile Insect Technique (examples from the Diptera) THEORY- BASIC SCIENCE APPLICATION 2- appreciate the variety and complexity of Insect sexual behavior and the potential challenges of preserving “wild-type” behavior through mass- rearing techniques and quality control. 1- examine the evolution of sexual behavior ( the relationship between the distribution of resources females use and the behaviors males employ to find and court females

2. Emlen and Oring, 1977 -A simple beginning- “all other things being equal” • When resources are rare relative to females, then females are likely to be found near resources. • If resources are small relative to males, then a male may be able to control which other flies can use a resource.

3. Emlen and Oring Variables

4. Females predictable- resource undefendable Consequences 1- males find females near or on resource 2- limited male-male interactions- little selection for large males and little sexual dimorphism 3- Females have few opportunities to escape male attentions and so little selection for male courtship- simple precopulatory behaviors

5. Phoretic Norrbomia frigipennis on the ball-rolling scarab Canthon pilularis Such flies are locally common and where they occur nearly all dung beetles will bear phoretic “kleptoparasites”in groups of up to a dozen or more. Sivinski, 1984

6. Norrbomia frigipennis on Phanaeus vindex Flies are reluctant to leave their “hosts” and remain with the beetle as it burrows underground and even in flight Sivinski, 1982

7. What the world calls good business is only a way to gather up the loot, pack it, make it more secure in one convenient load for the more enterprising thieves. Chuang Tzu, 250 B.C. Females ride to reach subterranean dung storage sites Males and copulations are common on beetles No sexual dimorphism and no obvious courtship Sivinski, 1984

8. Emlen and Oring Variables

9. Females predictable- resource defendable consequences 1- males find females at resources 2- advantagous for males to control access to resource and so control access to females- selection for large male size and “weapons” 3- expensive for females to discriminate among males- little selection for male courtship

10. Phytalmia cervicornis (Tephritdae) Females of this genus lay their eggs in “pin-sized” holes in particular species of freshly fallen trees- a rare and easily defended resource. Males bear “antlers” similar to deer, but females are hornless (or nearly so) Sivinski, 1997

11. Phytalmia mouldsi (Tephritidae) A male with its antlers removed is treated like a female by a rival male Photo by Gary Dodson

12. Zygotricha dispar (Drosophilidae) In addition to antlers there are other peculiar modifications of the head in resource-defending flies (usually involving the eyes) Sivinski, 1997

13. Achias sp. (Platystomatidae) eyes Eleven families of acalypterate flies have stalk-eyes or some other extension of the head What might have begun as a propaganda tool passing misinformation may now be an honest advertisement of prowess Sivinski, 1997

14. Emlen and Oring Variables

15. Females unpredictable- resource defendable consequences There is little reason for a male to defend a resource if a female in unlikely to visit it- but If foraging females can be attracted to the resource it may become worth the effort 1- selection for male long-distance signals to females from resource sites 2- females have greater freedom to avoid unwanted males and male courtships (“advertisements”) are more elaborate

16. Female Papaya Fruit FlyToxotrypana curvicauda The long ovipositor allows the female to bypass the chemically defended pulp and lay her eggs among the seeds in the fruit’s center

17. Papaya Fruit FlyLarvae Larvae feed on seeds rather than fruit pulp

18. Adult Male Papaya Fruit Flies, Pheromone glands – pheromones are typically produced by female insects- only 5% or so by males and usually by males that occupy a resource site. Photo in Nation, 2003

19. Emlen and Oring variables

20. Females unpredictable-resources undefendable Consequences 1- males no longer remain for extended periods with an individual resource site (kleptoparasites of predaceous insects)

21. Acalypterate flies feeding on the prey of a large spider (Nephila clavipes) Unlike phoretic flies on dung beetles, the flies closely associated with arthropod predators are generally rare and almost always female. Sivinski et al., 1999

22. An unusual sight- Olcella quadrivittata (Chloropidae) mating on the prey of a robber fly (Asilidae). Species of this genus are among the most commonly encountered (and hence predictable) kleptoparasites. In common species It is worthwhile to wait by predators (or respond to predation cues such as defensive compounds) because females are likely to be found on prey Sivinski et al., 1999

23. Females unpredictable- resources undefendable Consequences 1- males and mating no longer associated with individual resource 2- males may search for mates and females may be selected to give “inexpensive” aid (bioluminescence in fungus gnats)

24. Orfellia fultoni (Mycetophilidae) Certain predaceous fungus gnats produce webs, some containing poison droplets (oxalic acid), in order to capture prey. Several genera have independently evolved light organs Harvey, 1952

25. Orfellia fultoni (light organs) Among insects, blue lights are found only in the bioluminescent mycetophilids- but have arisen apparently independently within a single subfamily at least 4 times Sivinski, 1980

26. Arachnocampa luminosa (Mycetophildae) An adult fungus gnat emerges from it puparium. Female pupae are brighter than male and glow even brighter when touched. Adult females briefly remain luminous after emergence Males appear to search for lights that might reveal a potential mate.

27. Females unpredictable- resource undefendable Consequences 1- males and mating no longer associated with individual resource 2- males may search and females give “inexpensive” aid 3- males may signal- if so, signals are relatively “expensive” and females free to discriminate among male advertisements (females are now “free” to leave- resources are relatively common and unlikely to contain a male)

28. courtship in the ulidiid Physiphora demandata Portions of one of the most complex series of insect courtship displays Females oviposit in detritus, a relatively homogeneous resource that does not concentrate females and is difficult for males to control Females are “free to leave” and males “convince” them to stay and mate Alcock & Pyle, 1979

29. Midleg of the male mosquito Sabathes cyaneus Apparent sexual displays are often on the legs of flies Ornaments are rare among mosquitoes Male S. cyaneus fly toward resting females with their legs held perpendicular to their bodies. After landing they hang by their front legs and wave their paddles. Sivinski, 1997

30. The forelegs of male dolichopodid flies Dolichopus pulchrimanus The range of ornamentation on the legs of Dolichopodidae (the “long- legged” flies) Campsicnemus magius Sivinski, 1997

31. What do “ornaments” and other signals mean? 1- run-away selection (“fashionable” ornaments) 2- receiver bias (exploitation of female perceptions) 3- good genes (good sense vs good taste) 4- indications of investment (nuptial gifts- exaggeration and eventual honesty in empidid flies)

32. Midleg of the male empidid Rhamphomyia scaurissima Sivinski, 1997

33. Male “ornamented” empidid Rhamphomyia scaurissima Male R. ursinella with a nuptial gift, Smittia sp. gnat Might the ornament resemble a nuptial gift or exaggerate the size of a small offering? Sivinski, 1997

34. Female Rhamphomyia longicaudata (Empididae) with inflated abdomen Females of a number of empidid genera exaggerate their abdomens (in this case swelling the abdomen with air) Were these originally attempts to exaggerate fecundity and obtain nuptial gifts from choosey males? Steyeskal, 1941

35. Females predictable- resources undefendable consequences 1- males no longer associated with individual resource 2- males may search and females provide inexpensive signal 3- males may signal- but will be expensive and females free to discriminate 4- males, or rarely females, may form mating aggregations

36. Mating aggregations-swarms and leks 1- Hot spots- non-resource based female concentration (over-lapping female home ranges or navigational clues) 2- Hot shots- accumulations in the vicinity of attractive males 3- Safety in sexual selfish-herds- female preference for a location within lek 4- Female best able to discriminate among grouped males

37. Signals within swarms (several pest insects, including mosquitoes, swarm) Mate choice in swarms poorly understood Rapid flight in a group makes individual recognition difficult Male signals are rare and more dramatic examples occur in species with slow or stationary flight

38. A swarm of unidentified nematoceran flies – the serious difficulty of identifying individual signalers

39. Hindleg of the swarming Calotarsa insignis (Platypezidae) An ornamented species that hovers within its swarm, dangling aluminum-colored leg ornaments Kessel & Maggioncalda, 1968

40. Balloon flies (Empididae) at twilight

41. Lek of the Hawaiian Drosophila heteroneura (Drosphilidae) LEKS Thornhill and Alcock, 1982

42. Signals in leks Territories on leaves and other surfaces are stable stages on which to perform individually recognizable signals and this can result in diverse and intense displays (leking tephritid fruit flies)

43. A mating aggregation in the Caribbean fruit fly Anastrepha suspensa. > Males hold territories on the leaves (not the fruit) of host plants > Males defend territories from sexual rivals > Males communicate with potential mates through pheromones, acoustic signals and visual displays.

44. Eversion of the anal membrane during pheromone emission J. L. Nation, 1989

45. Deposition of Anastrepha suspensa pheromone components Putting pheromone on leaf increase the area of the emission surface Sivinski et al., 1994

46. Since pheromones are deposited on leaves, territories may acquire value with use- one reason males fight to possess signal sites

47. Relationship between pheromone deposition and wing-fanning There is a positive correlation between the number times a male touches his anal-pheromone gland to a leaf surface and the movement of his wings Sivinski, Epsky, & Heath, 1994

48. Pulse Train from the Calling Songs of the Caribbean Fruit Fly J. Sivinski, & J. C. Webb, 1985

49. Capture of female A. suspensa in traps baited with live males, pheromones, and recorded acoustic signals Females can be attracted by recorded song alone Webb, Burk and Sivinski, 1983

50. Outcomes of Female Mate Choice Experiment (One Large vs. One Small Male) Caribbean Fruit Flies (Anastrepha suspensa) Females prefer large, calling males over small, non-calling males Burk & Webb, 1983