Robert A. Krebs and Karen L. Bean.
The mating behavior of Drosophila mojavensis on organ pipe and agriacactus.
Psyche 98(1):101-109, 1991.

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THE MATING BEHAVIOR OF DROSOPHILA MOJAVENSIS ON ORGAN PIPE AND AGRIA CACTUS
BY ROBERT A. KREBS~ and Karen L. Bean
Department of Zoology, Arizona State University Tempe, AZ 85287- 1501
Drosophila flies are prime examples of laboratory animals that have been poorly studied in nature. This is true even for the cac- tophilic members of the genus, for which the breeding habitat is well known (Barker and Starmer, 1982; Barker et al., 1990; although see Markow, 1988). One of four cactophilic Drosophila endemic to the Sonoran Desert, D. mojavensis, utilizes primarily necrotic tissue of agria cactus, Stenocereus gummosus, on Baja California and organ pipe cactus, Stenocereus thurberi, in main- land Sonora, Mexico and southern Arizona (Fellows and Heed, 1972; Heed, 1978).
Isolated populations of D. mojavensis show morphological, behavioral and genetic variation, (Mettler, 1963; Zouros, 1973; Etges, 1989 Krebs, 1990), features that have made this organism important for studying the evolution of reproductive behaviors and speciation. Populations on the Baja peninsula and mainland Sonora, Mexico are separated by the Gulf of California, and labo- ratory experiments have shown partial sexual isolation between them (Wasserman and Koepfer, 1977; Koepfer, 1987a, 1987b; Krebs and Markow, 1989).
Despite the great attention given this species for evolutionary studies, knowledge of its behavior in nature is limited to prelimi- nary tests of dispersal (Johnston, 1974), rearing records from necrotic cacti returned to the laboratory (Heed and Mangan, 1986; Ruiz and Heed, 1988), and a brief mention of adult distribution on organ pipe (Markow and Toolson, 1990). This deficiency led us to study the behavior of D. mojavensis on organ pipe and agria cactus current address: Department of Animal Science, University of New England, Armidale, New South Wales 235 1, Australia Manuscript received by the editor December 4, 1990.



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102 Psyche [vo~. 98
to demonstrate that results obtained in the laboratory are applica- ble to populations in nature.
MATERIALS AND METHODS
Observations of D. mojavensis were performed on two popula- tions of the mainland Sonora race. One site was a population ca. 20 km south of Ajo, Arizona where organ pipe cactus is plentiful on the southern and eastern slopes of the St. John the Baptist Moun- tains (the St. John site). A second population was observed that uses agria cactus in the Desemboque region of Sonora, Mexico, approximately 30 km north of Punta Chueca, across from Tiburon Island.
Drosophila mojavensis adults may be watched easily on the outer skin and within pockets of necrotic cactus arms (rots). We found that the number of flies on the necrotic arms varied, as rots of typical appearance often contained no flies whereas apparently less promising rots had many. The number of necrotic arms at the Desemboque agria site was greater than at the organ pipe site, as is typical for these two cacti (Mangan, 1982). More flies were pre- sent at the agria site, but they were spread over many plants. We found most flies at a single rot at the organ pipe site. Observations were recorded periodically through Oct., 1988 to March, 1989 (Table 1), during which we made continuous observa- tions on flies for three hours beginning at sunrise (ca. 7 AM) and again for two hours before sunset (ca. 5:30 PM). Rots were also examined for the presence or absence of flies and courtship behav- ior throughout the day.
Table 1. Number of matings and vertical distribution of copulating pairs of Drosophila mojavensis along an upright columnar cactus arm. Number of Vertical
Date matings distribution (em)
1 012218 8 13
35
10123188 23
5 0
11/5/88 60
110
1 1/6/88 22
8 5
2/26/89' 9
25
3/9/89 1
10
Observations made on agria cactus




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199 11 Krebs & Bean
Courtship behavior
Courtship and mating were common from shortly after sunrise until 10:00 AM during Autumn to early Spring. On organ pipe, few flies were observed at rots during the afternoon, and although a few males were observed on rots shortly before sunset (5:OO PM), little courtship and no copulations were observed. Courtship components on the cactus were identical to those observed previously in the laboratory (Markow, 198 1). Males courted females from the rear, while intermittently vibrating one or both wings. During courtship, the male's foretarsi drummed contin- uously upon the underside of the female's abdomen. Successful males elicited a characteristic acceptance signal, wing spreading by the female, that was followed by an immediate attempt to mount. The courtship durations measured in the field ranged from a few seconds to over a minute before female acceptance or rejection.
Female acceptance signals usually led to successful copulation. Of 30 attempted copulations observed, three males failed to copu- late. They fell off the female and dropped to the ground, unable to resume courtship with the same female. During copulation the flies remained motionless unless greatly disturbed. If other males courted the copulating pair, the female usually walked away with the male in copula. We never observed D. mojavensis fly while in copula.
Physical conflict between males was never observed unless two or more males courted the same female. A male that approached a courting pair would push between them from the side to gain access to the female's ovipositor. The interrupting male initiated courtship immediately, ignoring the previous male, but no inter- rupted courtship led to successful copulation. Mating System
Drosophila mojavensis males on necrotic cactus arms generally remain motionless unless disturbed by the arrival of a female. Some males were positioned just within or at the edge of breaks in the cactus skin that allowed females access to necrotic tissue, but the majority were distributed across the necrotic cactus arms, far from openings to oviposition sites. On agria cactus, we observed



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104 Psyche [vo~. 98
some matings on non-necrotic arms, but all observed matings on organ pipe were on the arm containing the necrotic tissue. A test for random male spacing was performed by overlaying the positions of males across the cactus arm, determined by pho- tographs (e.g., Figure I), on a grid. Randomness of male positions was compared to that expected under a Poisson distribution. The variance in male distribution was only 60 percent that of the mean indicating a repulsed distribution. Males were spaced more evenly than expected by chance.
Although D. mojavensis males present at high densities were evenly dispersed across the cactus arm, at lower densities males were concentrated adjacent to openings to the necrotic tissue. The vertical distance of an upright cactus arm over which males were perched, their vertical distribution, was positively correlated with the number of observed matings (Table 1, r=0.91, P<0.01). For the two days with the lowest number of observed matings and for additional observations of rots with only few males and no mat- ings, most flies remained by the rot entrance. The total number of flies on rots, however, could not be measured because females, and possibly males as well, continuously arrive and depart during mat- ing periods.
The horizontal distribution of flies was influenced by factors different from those affecting the vertical distribution. Males were expected to wait (1) on the leeward side to intercept landing females which presumable fly upwind to the necrotic cactus arm, following volatile cues (Fogleman, 1982) or (2) along the side of the cactus arm containing the opening to the rot to more easily intercept females walking to oviposition sites. During observations on an arm fully exposed to the sun (November 5th and 6th, beginning at sunrise, ca. 7 AM), half of the observed matings in the first hour took place in direct sunlight (1 1 of 21, excluding any that occurred within the rot pocket). After 8:00, almost all males moved to the shaded side of the cactus and Figure 1. The distribution of males of Drosophila rnojavensis at relatively high densities on part of an upright necrotic arm of organ pipe cactus (reproduced from a photograph taken shortly after sunrise, Nov. 5, 1988). As the entire arm rots and turns brown, the spines and areoles may break off, providing possible access to the soft necrotic tissue, indicated by the small solid black regions in the center. Larger and more accessible openings in the cactus were located on the opposite side. Densely speckled areas on the right represent slowly flowing exudate which is used as feeding sites on the surface.




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106 Psyche [VOI. 98
only 1 of 59 observed matings occurred in direct sunlight (G=46.7, Pc0.001). In contrast, where a rot was shaded by other arms of the plant (Oct. 22 and 23), all observed copulations (N = 36) occurred within 5 cm left and right of the only entrance point through the cactus skin, although the vertical distribution of males was much greater (Table 1). Temperature and access to the rot were therefore most important to the distribution of males. Courtship structure of D. mojavensis is similar in the field and in the laboratory. Only the cost to males of failing to successfully mount receptive females is substantially different between the lab- oratory and the field. In the laboratory, failure to copulate after female acceptance is observed for 18 percent of copulation attempts, but males reinitiate courtship and almost always mate eventually (Krebs and Markow, 1989).
Laboratory observations showing an absence of direct male- male aggression, expected where no male size advantage in mating is present (Krebs and Markow, 1989), were supported in the field. More than one male will attempt to court the same female, but con- tact between males appears incidental to gaining access to her ovipositor. As observed on the cacti, a female courted by two males in shell vials will rarely accept a male until one can court without interruption by another male (unpublished data). Laboratory results showing correlation between courtship latency and female locomoter activity (unpubl.) can be explained by the stationary posture of males at mating sites. On cactus, receptive females are active while sexually ready males are not. The mating system of D. mojavensis at relatively high densities is similar to that of D. nigrospiracula, which has been reported "lekking" on saguaro cactus (Markow, 1988). Drosophila nigrospiracula populations tend to be much larger than those of D. mojavensis, and most matings take place on non-necrotic portions of the saguaro. Our observations of D. mojavensis, however, sug- gest that the mating system may be labile, and that a resource defense mating system based around oviposition sites provides males with the greatest opportunity for mating when fly densities are low.




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Determination of mating periods may be deceptive in the labo- ratory where mature virgin flies may mate at any time. The mating sites in the field are not occupied throughout the day. Also, obser- vations made during evenings in late spring while collecting flies (Markow, pers. comm.) suggested two daily mating peaks, and multiple mating within a day are possible for D. mojavensis (Krebs, 1991). Both events, however, are unlikely during seasons of short day length. Darkness and falling temperatures may reduce mating opportunity before females again become receptive after mating in the morning.
Our observations of D. mojavensis show the importance of studying animals within their natural environment even when they can be easily maintained in the laboratory. Timing of behaviors differs in nature, and behaviors such as number of mating peaks, mate choice, and locomoter activity, are more easily interpreted following even a short field study.
The courtship behavior of Drosophila mojavensis under field conditions was similar to that observed previously in the labora- tory. Males were uniformly spaced across necrotic arms of organ pipe cactus when present at high densities, although aggregations were centered around openings to oviposition sites. At low densi- ties, most males were adjacent to these openings. The two daily mating peaks observed in the laboratory were reduced in the field to one during the mornings when day lengths were short. Previous observations on the behavior of D. mojavensis have been made by a number of investigators, Therese Markow of Ari- zona State, Henar Pimentel and Bill Heed at the University of Ari- zona, William Etges at Arkansas, and Tom Starmer of Syracuse. All shared their field experiences which aided our completion of this study. This project was supported by a small grant from the Arizona State Graduate Student Association.



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Psyche
[Vol. 98
BARKER, J. S. F. & W. T. STARMER
1982. Ecological Genetics and Evolution. The Cactus-Yeast-Drosophila- Model System. Academic Press, Sydney, Australia. BARKER, J. S. F., W. T. STARMER, & R. J. MACINTYRE 1990. Ecological and Evolutionary Genetics of Drosophila. Academic Press, N.Y. (in press).
ETGES, W. J.
1989. Evolution of developmental homeostasis in Drosophila mojavensis. Evol. Ecol. 3: 189-201.
FELLOWS, D. P. & W. B. HEED
1972. Factors affecting host plant selection in desert-adapted cactophilic Drosophila. Ecology 53: 850-858.
FOGLEMAN, J. C.
1982. Mating systems of cactophilic Drosophila, In: Ecological Genetics and Evolution. The Cactus-Yeast-Drosophila-Model System, eds. J. S. F. Barker and W. T. Starmer, Academic Press, Sydney, Australia. pp. 19 1-206.
HEED, W. B.
1978. Ecology and genetics of Sonoran desert Drosophila, In: Ecological Genetics: the Interface, ed. P. F. Brussard, Springer-Verlag, New York. pp. 109-126.
1982. The origin of Drosophila in the Sonoran desert. In: Ecological Genetics and Evolution. The Cactus-Yeast-Drosophila-Model System, eds. J. S. F. Barker and W. T. Starmer, Academic Press, Sydney, Australia. pp. 65-80.
HEED, W. B. & R. L. MANGAN
1986. Community ecology of the Sonoran desert Drosophila. In: The Genet- ics and Biology of Drosophila, Vol 3e, eds. M. Ashburner, H. L. Carson and J. N. Thompson, Jr., Academic Press, London, U.K. pp. 31 1-345. JOHNSTON, J. S.
1974. Dispersal in natural populations of the cactophilic Drosophila pachea and Drosophila mojavensis. Genetics 77: (supplement) 32-33. KOEPFER, H. R.
1987a. Selection for sexual isolation between geographic forms of Drosophila mojavensis. I. Interactions between the selected forms. Evolution 41: 37-48.
1987b. Selection for sexual isolation between geographic forms of Drosophila mojavensis. 11. Effects of selection on mating preference and propen- sity. Evolution, 41: 37-48.
KREBS, R. A.
1990. Courtship behavior and control of reproductive isolation in Drosophila mojavensis: analysis of population hybrids. Behav. Genet. 20: 535-543. 1991. Function and genetics of long versus short copulations in the cac- tophilic fruit fly, Drosophila mojavensis. Journal of Insect Behavior, 4: 221-233.
KREBS, R. A. & T. A. MARKOW
1989. Courtship behavior and control of reproductive isolation in Drosophila mojavensis. Evolution 43: 908-9 13.




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19911 Krebs & Bean 109
MANGAN, R. L.
1982. Adaptations to competition in cactus breeding Drosophila. In: Ecologi- cal Genetics and Evolution. The Cactus-Yeast-Drosophila-Model Sys- tem. eds. J. S. F. Barker and W. T. Starmer, Academic Press, Sydney, Australia. pp. 257-272.
MARKOW, T. A.
1981. Courtship behavior and control of reproductive isolation between Drosophila mojavensis and Drosophila arizonensis. Evolution 35: 1022-1 026.
1988. Reproductive behavior of Drosophila melanogaster and Drosophila nigrospiracula in the field and in the laboratory. J. Compar. Psychol. 2: 167-173.
MARKOW, T. A. & E. TOOLSON
1990. Temperature effects on epicuticular hydrocarbons and sexual isolation in Drosophila mojavensis, In: Ecological and Evolutionary Genetics of Drosophila, eds. J. S. F. Barker, W. T. Starmer and R. J. Maclntyre, Plenum Press, N.Y., pp. 3 15-33 1.
METTLER, L. E.
1963. D. mojavensis baja, a new form of the Mulleri complex. Dros. Inf. Ser. 38: 57-58.
RUIZ, A. & W. B. HEED
1988. Host-plant specificity in the cactophilic Drosophila mulleri species complex. J. Anim. Ecol. 57: 237-249.
WASSERMAN, M. & H. R. KOEPFER
1977. Character displacement for sexual isolation between Drosophila mojavensis and Drosophila arizonensis. Evolution 31: 8 12-823. ZOUROS, E.
1973. Genic differentiation associated with the early stages of speciation in the mulleri subgroup of Drosophila. Evolution 27: 601-621.



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