Mate selection by female katydids (Orthoptera: Tettigoniidae, Conocephalus nigropleurum)

Anita. Behav., 1982, 30, 734-738

MATE SELECTION BY FEMALE KATYDIDS (ORTHOPTERA: TETTIGONIIDAE, CO NOCEPHAL US NIGR OPLE UR UM) By DARRYL T. GWYNNE*

Department of Biology, University of New Mexico, Albuquerque NM 87131, U.S.A. Abstract. Female katydids receive a large spermatophore at mating which they subsequently eat. Available evidence indicates that spermatophore nutrients are important to female reproduction. Heavier males produce larger spermatophores. When given the choice between two singing males of different weights, females always mated with the larger individual.

In his theory of sexual selection, Darwin (1871) suggested that both male-male competition and female choice of mates result in non-random differential reproduction by males. The role of female choice remains controversial, in part because there is little direct evidence that females do choose certain conspecific males over others. In addition, few studies have demonstrated that females accrue advantages (i.e. adaptive mate choice) as a result of their choice of males (Thornhill 1980). Females are expected to be the more discriminating sex because of their relatively high investment in individual offspring. In species in which males provide resources to the female and/or her offspring, one of the criteria females should use to select mates is the quality or quantity of the resources that the male is likely to provide (Trivers 1972; Halliday 1978). Males of certain species of insects provide nutrition to the female during mating (Thornhill 1976a). In hangingflies (Mecoptera: Bittacidae), males provide the female with a prey arthropod which she feeds on during mating. Studies by Thornnill (1976b, 1978) have demonstrated that female hangingflies make adaptive choices of mates in that they choose males with large prey items, resulting in advantages associated with the number of eggs laid and a decreased risk of predation because females spend less time seeking their own food items. One of the commonest ways that male insects provide nutrients to the female is via products from salivary or reproductive accessory glands (Thornhill 1976a; Leopold 1976). Examples are known from several orders, most notably Lepidoptera (Boggs & Gilbert 1979) and Orthoptera. In the Orthoptera, there is a diversity of male-produced nutrition which is fed to females, and there is good evidence of subsequent *Presentaddress: Departmentof Zoology,The University of Western Australia, Nedlands, W.A. 6009, Australia.

reproductive benefits to these females. Males of some acridid grasshoppers introduce specialized proteins into the female's reproductive tract during copulation. These proteins are incorporated into the female's ovaries (Friedel & Gillott 1977). In many crickets (Gryllidae), females feed on both glandular products and the spermatophore after it has been voided of sperm (Alexander & Otte 1967). Bell (1979) recently showed that feeding by females on the spermatophore and metanotal gland secretions of male tree crickets (Oecanthus nigricornis (Walker)) increased the number of eggs subsequently laid. In the katydids (Tettigoniidae), the spermatophore is a complex structure consisting of an ampulla, or sperm-containing area, and a spermatophylax, a large mass of protein which is visible exterior to the female's gonopore (Fig. I, Plate I) (Boldyrev 1915). The spermatophylax and the empty sperm ampulla are eaten by the female after copulation (see Rentz 1972) (Fig. 1B, Plate I). The spermatophylax, produced by male accessory glands, contains no sperm (Boldyrev 1915) and can be a significant male contribution, since it comprises as much as 20-30% of the male's body weight in some species (Busnel et al. 1956). Preliminary research has revealed that radiolabelled spermatophore proteins of the conocephaline katydid Orchelimum are used in both eggs and somatic tissues of females (Toolson & Gwynne, unpublished data). Because spermatophore proteins appear to be important to female reproduction, female katydids should select mates who are likely to provide large-sized spermatophores. This paper reports the results of a laboratory study with the black-sided meadow katydid (Conocephalus nigropleurum (Bruner); Conocephalinae which show that (1) larger males provide larger spermatophores, and (2) when given the choice 734

G W Y N N E : M A T E S E L E C T I O N BY F E M A L E K A T Y D I D S

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GWYNNE: MATE SELECTION BY FEMALE KATYDIDS between two singing males of different weights, females prefer to mate with the larger individual. Methods Subjects were obtained as eggs from the field and were reared to adulthood in the laboratory (details of rearing in Pipher & Morris (1974); Morris et al. (1978)). In order to determine the relationship between male body size and spermatophore size, 35 matings were staged by pairing females with single males, each female being released 50-60 cm from a singing male. Males were primarily virgins or individuals that had mated once. Two males that were used had mated twice previously. At least a week separated the matings of these males in order to avoid the effects of recent matings on spermatophore size (see discussion below). Twenty virgin females were used and were first mated between eight to 14 days after the final moult. Fourteen of these females were remated to different males. In choice trials, individual virgin females were placed with two males of different weights. In these experiments no male was used more than twice and mated males were used only once. The weight of each pair of males selected differed by at least 0.02 g. The weightof the larger male (0.161 • 0.01 g, N - - 12) ( X • SD) averaged some third greater than that of the small male (0.123 ~ 0.012 g, N = 12). The mean weight of singing males in the laboratory was 0.134 r~ 0.013 g (range, 0.109-0.164 g, N -----60).

735

Two preliminary choice trials were conducted by placing the females in a large cage with the singing males. In the other trials, however, a Y maze was used (Fig. 2). For each trial the larger of the males was randomly assigned to one of two 7-cm 2 screen cages which had open front~ to allow female access. The maze was designed (1) to be as close to the natural situation as possible, with the males singing from the tops of dry plant stems spaced a metre apart (the mean distance between singing male C. nigropleurum in the field (Morris 1967)) and (2) to reduce the complexity of the situation so that females were restricted in their choice to two males, each male having a similar mating history (i.e: recently unmated) and being equally accessible to t h e female. When both names were singing from within their cages, the female was released onto a central stick at a point 75 cm from each male (see Fig. 2). In most trials one or both males stopped singing before the female was mated. A trial was considered valid only if both males continued to sing until the female mated. The 12 trials reported here are those in which this criterion was met. Results Heavier male C. nigropleurum produce larger spermatophores. Figure 3 shows a significant positive regression of male-weight-loss after spermatophore production on male body weight. Most of this weight loss is due to the t

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BEHAVIOUR,

production of the large spermatophore (Fig. 1, Hate I). In all 12 choice trials, females mated with the larger male (~2 = 12.0, P < 0.01). In the last 10 trials the behaviour of the female on the Y maze was observed. In most of these trials (seven of 10) the female, after a short pause ( ) ? - - 1.36 rain, range 0.5-2.32), moved toward the large male and subsequently copulated with him. In the other three, however, she moved toward and made physical contact with the small male at least once before moving toward and mating with the large male. On one occasion the female actually coupled with the small male, then pulled away after 3.9 rain, before a spermatophore was passed, eventually coupling with the large male for a successful mating. Discussion

Increased feeding by female orthopterans on male-produced nutrition is known to enhance fecundity (in tree crickets (Bell 1979), see p. 734). Although it is not known just how nutrition from the katydid spermatophore affects fecundity, it has been shown that much of the labelled ~permatophore protein is found in both fertilized and unfertilized eggs (Toolson & Gwynne, unpublished data). Evidence that male spermatophores in katydids may be important for female reproduction comes from a field study of the decticine, Anabrus simplex Haldeman (the Mormon 'cricket') (Gwynne 1981). Population .04

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densities of this species can be very high and males in these populations rarely call more than 2 rain before females are attracted. Several females may fight for access to a singing male and males select only the large, more fecund females as mates. The suggested cause of this role-reversal in courtship behaviour is that the male's energetic contribution to his very large spermatophore (up to 27 ~ of body weight) may exceed the female's parental investment in eggs (see Trivers 1972) with the result that males may limit female reproduction (Gwynne 1981). Morris et al. (1978) recently showed that C. nigropleurum females prefer to move toward a recording of multiple males singing over that of a single mate. In nature, females may move into areas with the highest densities of singing males in order to have a greater choice of mates. Field studies of conocephaline katydids indicate that receptive females interact with several males; female Orchelimum nigripes Scudder were observed to move among and approach several singing males, often for an hour or more, before mating with one (Feaver 1977). Results from the present study support the hypothesis that these females are seeking the heaviest males, those likely to provide the largest spermatophores. However, the data are also consistent with the hypothesis that females select males of some modal size and not the largest male available. Females in the trials may, therefore, have simply been discriminating against smaller-than-average males (I. L. Heisler, personal communication). The mean weight of singing males in the laboratory was significantly greater than the mean of the small males used in the trials (t = 2.75, P < 0.01). However, although no attempt was made to select pairs of males from throughout the size range, it should be noted that in two trials the weight of the smaller male was greater than the mean singing male weight. Since these smaller males were not mated, the indication is that females are making a directional choice of mates. Some estimate of how much larger a spermatophore the females in the choice experiments obtained by selecting large males over small ones can be determined from the regression equation for Fig. 3. The equation predicts that a male with the small mean weight (see Methods) would lose 0.012 g during mating. The actual mean weight lost by large males was 0.022 g (so = 0.005) (the equation predicts that a male of the large male mean weight would lose 0.020 g).

GWYNNE: MATE SELECTION BY FEMALE KATYDIDS K a t y d i d females should prefer heavier males b u t only if these have n o t recently m a t e d . Recently m a t e d male k a t y d i d s are k n o w n to p r o duce small s p e r m a t o p h o r e s ( F e a v e r 1977). S p e r m a t o p h o r e p r o d u c t i o n alone d r o p s the male c o n o c e p h a l i n e ' s weight b y a b o u t 10%, which m a y be detectable b y the discriminating female. A l t h o u g h there is some evidence (for Orchelimum nigripes) t h a t females in the l a b o r a t o r y can discriminate a g a i n s t newly m a t e d males ( F e a v e r 1977), in the field these newly m a t e d males are ousted f r o m o p t i m u m singing-perches (i.e. areas where females are likely to be encountered) b y heavier males, so females w o u l d r a r e l y c o n t a c t t h e m ( F e a v e r 1977). W h a t cues c o u l d the discriminating female be using to assess a m a l e ' s potential o f p r o v i d i n g a large s p e r m a t o p h o r e ? M o s t o f the females in the choice trials m o v e d straight to the larger o f the two singing males w i t h o u t c o n t a c t i n g the smaller one. A l t h o u g h the sample size is small, there is a n i n d i c a t i o n t h a t long-range cues, p r o b a b l y acoustical, are used in discriminating between males (see C r a n k s h a w 1979). L a r g e r males o f b o t h crickets ( F o r r e s t 1980) a n d c o n o c e p h a l i n e k a t y d i d s (Bailey & Thiele, in press) are k n o w n to have l o u d e r calling songs. I t is conceivable t h a t the female m i g h t use the a t t e n u a t i o n o f high song frequencies to separate the influences o f male size a n d distance on song intensity (see M o r r i s et al. 1976). Cues to weight used b y females after antennal c o n t a c t m a y come f r o m substrate v i b r a t i o n caused by t r e m u l a t i o n o f the courting male ( M o r r i s 1980). Acknowledgments T h a n k s to W i n Bailey, G a r y D o d s o n , L o r r a i n e Heisler, A l a n L y m b e r y , Jim Lloyd, G l e n n M o r r i s , R a n d y Thornhill, T o m W a l k e r a n d Bruce W o o d w a r d for c o m m e n t s a n d criticism o f the manuscript. T h e w o r k was s u p p o r t e d by a g r a n t f r o m N S F (BNS 7912208).

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Thornhill, R. 1980. Competitive, charming males and clmosy females: was Darwin correct? Flor. EntomoL, 63, 5-30. Triverz, R. L. 1972. Parental investment and sexual selection. In: Se~cual Selection and the Descent o f

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Man 1871-1971 (Ed. by B. Campbell), pp. 136-179. Chicago: Aldine. (Received 31 March 1981 ; revised 10 December 1981 ; MS. numbar: A2633)