The formation, transfer, and fate of spermatophores in Photinus fireflies (Coleoptera: Lampyridae)

E.D. van der Reijden, Jeff D. Monchamp, and Sara M. Lewis

Abstract: Fireflies in the genus Photinus have been assumed previously to be among the many insect species in which males transfer primarily sperm during mating. In this study, male P. ignitus and P. marginellus were found to produce a complex proteinaceous spermatophore in four paired male accessory glands, a major component of the spermatophore being formed within prominent spiral glands. The spermatophore is transferred to the female within the first 40 min of copulation, and sperm bundles are released into the spermatheca. The remainder of the spermatophore subsequently undergoes digestion within a specialized sac in the female reproductive tract. To examine the function of male sperrnatophores, male P . marginellus were fed rhodamine B, resulting in the production of intensely fluorescent sperrnatophores. After mating with rhodamine-dyed males, females incorporated material derived from male spermatophores into their oocytes within 58 h post mating. Nutrient donations from males during mating are expected to play particularly important roles in female oogenesis i i insects with nonfeeding adults, such as Photinus spp. The presence of spermatophores in Photinus is related to marked differences among species in their life histories, mating systems, and mating behaviors.

RCsumC : Les lucioles du genre Photinus comptent parmi les insectes reputes transferer surtout du sperme au cours de la copulation. Au cours de cette etude, nous avons constate que les miles de P. ignitus et de P. marginellus genttrent un spermatophore proteine complexe dans quatre glandes accessoires paires, la plus grande partie dans des glandes spiralees de grande taille. Le spermatophore est transmis a la femelle au cours des 40 premittres minutes de la copulation et des faisceaux de spermatozoi'des sont liberes dans la spermathttque. Le reste du spermatophore est par la suite digere dans une poche specialisee du systttme reproducteur de la femelle. De la rhodamine B a ete administree en nourriture des miles de P. marginellus et le r81e fonctionnel de leur spermatophore ainsi devenu fluorescent a pu etre etudie plus en detail. Cinquante-huit heures aprtts accouplement a des miles colores a la rhodamine, les femelles contenaient des produits derives du spermatophore dans leurs ovocytes. La transmission de matitres nutritives par les miles au cours de l'accouplement joue probablement un r8le particulittrement important, puisqu'elle favorise l'ovogenttse chez des femelles d'insectes qui ne se nourrissent pas au stade adulte, comme les lucioles du genre Photinus. La presence de spermatophores chez Photinus est associee a des differences specifiques marquees de leur cycle, de leur systttme copulateur et de leur comportement au cours de la copulation. [Traduit par la Redaction]

Introduction Here we report that in two Photinus species, males produce

Numerous studies have provided insight into the biolumines- cent flash communication systems used during courtship by lampyrid beetles (e.g., Lloyd 1966; Papi 1969; Buck and Buck 1972; Copeland and Mosieff 1995; Branham and Greenfield 1996). However, relatively little is known concerning lampyrid copulatory behavior or reproductive anatomy (but see Wing et al. 1983; Wing 1984, 1985; Lewis and Wang 1991). Within the genus Photinus, the functional significance of species differences in male external genitalia (Green 1956) is unknown, and features of internal reproductive anatomy are known for only two species (Wing 1985). These fireflies have previously been assumed to be among the many insect species in which males transfer free sperm during mating.

Received August 30, 1996. Accepted February 12, 1997.

E.D. van der Reijden. Department of Zoology, University of New Hampshire, Durham, NH 03824, U.S.A. J.D. Monchamp and S.M. Lewis.' Department of Biology, Tufts University, Medford, MA 02 155, U.S .A.

' Author to whom all correspondence should be addressed. (e-mail : slewis 1 @tufts.edu).

a complex proteinaceous spermatophore that is transferred to the female during copulation. Following release of sperm into the spermatheca, the spermatophore subsequently under- goes digestion inside a specialized gland within the female reproductive tract.

Spermatophores consist of sperm packaged within a struc- ture produced by the male accessory glands, and are found across a remarkable range of animal taxa (reviewed by Mann 1984). While spermatophores are likely to have originally served for sperm protection and transport (Davey 1960; Mann 1984), a secondary function appears to have evolved in a number of insect taxa. In many insects, nutrients derived from male spermatophores are used by females for reproduc- tion and somatic maintenance (reviewed by Zeh and Smith 1985; Simmons and Parker 1989; Boggs 1990). A theoretical model developed by Boggs (1990) predicts that spermato- phore-derived nutrients will be particularly important in female oogenesis in insects with nonfeeding adults, such as Photinus spp. In this study we examine the functional role of the spermatophores of Photinus spp. by mating females with males that had been fed rhodamine B dye. The distribution of lluorescent, rhodamine-dyed material was then monitored at various times following copulation.

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Materials and methods

Photinus ignitus and P. marginellus are both widely distributed in eastern North America (Lloyd 1966). Adults were collected from field sites in Middlesex County, Massachusetts, U .S. A. (Concord, Lincoln, Medford, and Weston), and Rockingham County, New Hampshire, U.S .A. (Barrington). Species identifications were based on male genitalia (Green 1956) and flash behavior (Lloyd 1966) and were confirmed by Dr. J.E. Lloyd. Fireflies were maintained indi- vidually in plastic containers with pieces of apple, which is ingested by both sexes in the laboratory (Lewis and Monchamp 1994).

To examine reproductive anatomy, fireflies were anesthetized with carbon dioxide or by cooling, then decapitated and dissected in insect saline (P. ignitus: 16 males and 21 females; P. marginellus: 9 males and 19 females). Copulation anatomy was examined by placing a male and female together and monitoring them continu- ously until mating occurred. General characteristics of mating anatomy were noted for 11 P. ignitus pairs dissected at various times after the beginning of copulation stage I1 (following the behavioral description of Lewis and Wang 1991). The time course of spermatophore transfer in P. margirlellus was determined by dissecting mating pairs 15, 30, 45, and 60 min after the beginning of copulation (n = 2 for each time interval).

To examine the fate of the spermatophore, female P. marginellus mated with rhodamine-dyed males were dissected at various times after copulation. Male P. marginellus were fed rhodamine B, a fluorescent thiol-reactive dye that forms a stable covalent bond to proteins (Sigma Chemical Co.; excitation maximum 540 nm, emis- sion maximum 625 nm). Rhodamine B is known to stain male spermatophores (Sparks and Cheatham 1973). Before mating, males were supplied with sucrose crystals and 4.17 x l o p 3 M rhodamine B on paper towels. Rhodamine B ingestion appeared to shorten the I ife-span of males (undyed males: 1 1 f 1.3 days (mean f 1 SE), n = 35; dyed males: 7 +_ 0.5 days, n = 25; t = 2.2, p < 0.025), but had no apparent effect on their mating behavior. Rhodamine-dyed (dark purple) males were mated singly to undyed females. After mating, females were maintained with apple pieces and randomly assigned for dissection 10, 34, or 58 h after the end of copulation to examine reproductive structures for fluorescence intensity (n = 2 for each time interval). The entire female reproductive tract was dissected out and observed with a Nikon Fluophot micro- scope using the built-in IF420-490 and auxiliary filters. Fluores- cence was ranked from 0 (no fluorescence) to 6 (highest intensity).

Results

Female reproductive system In female P. ignitus, numerous oocytes at different develop- mental stages are present within each ovary (Fig. 1). Females contained between 0 and 44 mature oocytes (defined as oocytes r 600 pm diameter) generally located in the lateral oviducts or in the proximal end of the ovarioles. The lateral oviducts leading from each ovary join together to form a short common oviduct that enters the bursa dorsally about halfway along its length. A flattened, elongate accessory gland empties into the bursa opposite the common oviduct opening.

The female bursa copulatrix is bordered by two hemi- sternites, and a sclerotized plate is attached to the ventral wall of the bursa near the genital opening. At the anterior end of the bursa is a hemispherical spermatheca with a highly rugose, convoluted surface (Fig. 1). The inner base of the spermatheca is encircled by a rigid transparent rod, the two ends of which join to form a funnel-shaped channel. This channel extends through the wide spermathecal duct, taper- ing to a narrow end within the bursa in the vicinity of the

common oviduct. In P. ignitus there are generally one to three distinct pouches within this bursal channel that are covered by secretory cells, overlaid in turn by a dense concentration of fat body.

Also located at the anterior end of the bursa is a thin membranous sac in which spermatophore digestion occurs. In field-collected females, this spermatophore-digesting gland (SDG) is generally collapsed (see Fig. 1). It often contains an opaque amorphous mass that appears to represent the remnants of one or more spermatophores after digestion, and includes crystalline material similar to that secreted by the male short accessory glands.

The female reproductive anatomy in P. marginellus is similar to that of P. ignitus, although spermathecal size is reduced relative to body length. In addition, the bursal plate of P. marginellus is more deeply notched along its anterior margin.

Male reproductive system In male P. ignitus, the paired testes are spherical and bright pink and lie below the second and third abdominal segments. The tubular vasa deferentia lead to the seminal vesicles, which are represented by a dilation of the proximal end of these ducts (Fig. 2). The seminal vesicles enter the ejacula- tory duct at its junction with the accessory glands. Sperm produced in the testes are coiled into sperm bundles (Fig. 3) that are approximately 70 pm in diameter and composed of 50 - 100 sperm, each about 1 80 pm long.

The male reproductive system in.P. ignitus is character- ized by four pairs of elaborate and conspicuous accessory glands. The most prominent accessory glands (Figs. 2 and 3) are the tightly coiled. paired spiral accessory glands that are aligned longitudinally within the abdominal cavity and are approximately 1.5 mm long and 0.5 mm wide. These spiral glands each contain an opaque spiral secretion represent- ing half of the prespermatophore, each half bearing two longitudinal rows of pyramidal scales (Fig. 3).

Males have three additional pairs of transparent tubular accessory glands that appear structurally similar but vary in length. The paired long accessory glands are thin-walled, coiled tubes that are 18 -24 mm in length when uncoiled and 100-200 pm in width. The paired medium accessory glands are similar in width but range in length from 5.2 to 6.6 mm. The products of the medium and long accessory glands appear as a granular secretion that occupies scattered por- tions of the gland lumen. The short accessory glands are 1 .O-1.3 mm long and produce an opaque white secretion containing crystalline material.

The spiral glands and short accessory glands join the ejaculatory duct from the dorsal side at the same level as the seminal vesicles (Fig. 2). The long and medium accessory glands enter laterally into the ejaculatory duct distal to the seminal vesicles. The ejaculatory duct emerges through the short median lobe of the male aedeagus. The aedeagal morphology of P. ignitus is similar to that of other mem- bers of the P. consangiiineus complex (Green 1956), with ventrobasal processes on the median lobe and two short, heavily sclerotized lateral lobes.

The internal reproductive anatomy of male P. marginellus is quite similar, except that all accessory glands are cor- respondingly smaller in these smaller fireflies. In P. mar-

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Figs. 1-4. Female and male reproductive anatomy of Photinus ignitus and P. marginellus. Scale bars: 500 pm in Figs. 1-3; 250 pm in Fig. 4. Fig. 1. Reproductive system of a female P. ignitus, with mature oocytes visible within the lateral oviducts (LO). Oocytes at several developmental stages are in terminal ovaries (Ov). The flattened accessory gland (Ac) enters the bursa copulatrix (Bc) opposite the common oviduct. Sperm are stored in the spermatheca (St) located at the anterior end of the bursa copulatrix. Male spermatophores undergo digestion within the spermatophore-digesting gland (SDG), which is collapsed here. The bursal plate is not visible. Fig. 2. Reproductive system of a male Photinus ignitus, dorsal view; a prespermatophore (pSph) is contained within the spiral accessory glands (SpAG). Spiral glands and seminal vesicles (SV) lead into the ejaculatory duct (E), along with the tubular short accessory glands shown flanking the ejaculatory duct (the long and medium accessory glands are not visible). Fig. 3. Spiral accessory gland of a male Photinus ignitus, containing the prespermatophore (pSph) with a row of pyramidal scales (arrowhead). Sperm bundles can be seen within and leaking from the seminal vesicle (SV). Fig. 4. Mating anatomy of Photinus marginellus 30 min after the beginning of copulation. The pair is tightly coupled, with the lateral lobes of the male aedeagus (A) hooked over the female bursal plate (P). A spermatophore (Sph) is extruded from the male ejaculatory duct into the greatly distended spermatophore-digesting gland (SDG). A mass of sperm bundles (S) has been forced out of the spermatheca (St) by cover-slip pressure.

SpAG

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ginellus, the aedeagal morphology is different (Green 1956), and is characterized by a long, acutely pointed median lobe and two slender arched lateral lobes bearing hooked ends.

Prior to mating in both species, the two halves of the prespermatophore are clearly visible within the male spiral glands (Figs. 2 and 3), sperm bundles fill the seminal vesicles (Fig. 3) and vasa deferentia, and the three pairs of tubular accessory glands contain granular secretions. The gland con- tents are depleted immediately after mating, but the sperma- tophore components are replenished within 24 h post mating.

Copulation anatomy and spermatophore transfer The median duration of copulation in P. rnarginellus is 91 min (Lewis and Wang 1991). Within 15 min after the initiation of mating in P. rnarginellus, the pair is tightly coupled, with the lateral lobes of the male aedeagus hooked over the bursal plate of the female. The distal end of the male ejaculatory duct is extended inside the bursa nearly to the base of the common oviduct. The end of the ejaculatory duct appears to be anchored in the bursal wall by minute spines along its exterior surface. Within the male the two halves of the prespermatophore have emerged from the spiral glands and joined together to form the major structure of the sper- matophore within the male ejaculatory duct. The tubular accessory glands of the male are empty.

Spermatophore transfer to the female occurs within 30 min following the beginning of copulation (Fig. 4). The sperma- tophore consists of a spirally coiled gelatinous tube, approxi- mately 2 mm long and 0.1 mm wide, covered by a transparent sheath. The spermatophore enters the female SDG, which becomes markedly distended. By 30 min, sperm bundles have been deposited in the female spermatheca from the anterior end of the spermatophore.

By 45 min, the spermatophore is located completely within the SDG and remains largely intact, with the pyramidal scales formed by the male spiral glands still clearly visible. Sperm appear to become capacitated within the spermatheca, as sperm bundles disperse into a dense aggregation of loose sperm by 45 min.

Mating pairs remain coupled at 60 min, although sper- matophore transfer is complete and the ejaculatory duct has been retracted into the median lobe of the male aedeagus. The lateral lobes of the male aedeagus maintain contact with the bursal plate of the female, but pairs are easily separated.

A similar process of spermatophore transfer occurs in P. ignitus, although copulation lasts for several hours. Sperm bundles have entered the spermatheca, and spermatophore transfer occurs within 40 min after the beginning of copula- tion. By 1.5 h, the spermatophore is located within the SDG, and by 3.5 h the sperm bundles have dispersed and a dense mass of motile sperm is present in the female spermatheca. In male P. ignitus, the lateral lobes of the aedeagus are shorter than in P. marginellus and do not hook over the female bursal plate; P. ignitus mating pairs are more easily separated.

Fate of the spermatophore Rhodamine-dyed male P. marginellus dissected before mating showed intense fluorescence (rank 6) of their spiral glands (including prespermatophores), and the testes and tubular accessory glands were also moderately fluorescent (rank 4).

Table 1. Fluorescence rankings of reproductive structures of undyed female P. marginellus mated to rhodamine-dyed males measured at three postmating intervals (0 = no fluorescence, 6 = highest intensity).

Postmating interval (h)

Male spermatophore . Sheath 6 5 Digested Pyramidal scales 5 5 4

Female reproductive structures Spermatophore-digesting gland 4 3 -4 3 Spermatheca 2 3 3 -4 Developing oocytes 1 3 3 Mature oocytes 0 2-3 3

Undyed males as well as unmated females showed no natural iluorescence (rank 0). Female P. marginellus dissected 10-58 h after mating with rhodamine-dyed males had intensely fluorescent material transferred from the male in their reproductive tracts. Mere contact with males did not appear to result in dye transfer, as none of the mated females showed fluorescence of the bursa copulatrix (rank 0).

Ten hours after a female mated with a rhodamine-dyed male, the contents of the SDG were moderately fluorescent (Table I) and the spermatophore had begun to disintegrate. Sections of the spermatophore sheath showed intense fluores- cence visible through the SDG membrane. Pyramidal scales had become detached from the spermatophore and were strongly fluorescent within the SDG. The female spermatheca showed weak fluorescence, presumably from dyed sperm or other accessory gland products. While none of the mature oocytes fluoresced, all the developing oocytes uniformly showed fluorescence.

Thirty-four hours after mating, the SDG contents exhib- ited slightly weaker fluorescence relative to that after 10 h. Fragments of the partially disintegrated spermatophore sheath and pyradimal scales were still strongly fluorescent. The female spermatheca increased in fluorescence intensity. Within the ovarioles, developing oocytes increased markedly in fluorescence intensity and about a third of the mature oocytes had become fluorescent. The membrane surrounding the ovarioles showed no fluorescence (rank 0).

Fifty-eight hours after mating, the SDG contents had declined in fluorescence intensity. The spermatophore sheath had disintegrated almost entirely and the pyramidal scales showed somewhat reduced fluorescence. The spermatheca showed a slight increase in fluorescence intensity. Between 34 and 58 h, an increased proportion of mature oocytes, but not all, showed strong fluorescence, while all develop- ing oocytes showed fluorescence similar to that observed after 34 h.

Discussion

This study revealed several novel features of the reproduc- tive anatomy of Photinus spp. Males of two firefly species, P. ignitus and P. rnarginellus, manufacture complex sper-

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matophores from four paired accessory glands, with the prominent spiral glands forming the major structural compo- nent of the spermatophore. When male P. rnarginellus were fed rhodamine B, the intense fluorescence exhibited by both the spiral glands and the prespermatophore suggested that these structures have a high protein content. Multiple male accessory glands are found in many insects, and the roles played by different glands in spermatophore formation have been reviewed by several workers (Leopold 1976; Gillott 1988; Kaulenas 1992).

The male reproductive anatomy of both P. ignitus and P. rnarginellus described here is similar to that described for P. macdermotti in Florida (Wing 1985). Males of all three species possess spiral and tubular accessory glands. In P. macdermotti, Wing (1985) described a secretion from the spiral gland that, although not identified as such, is likely to represent a spermatophore similar to those described here for P. ignitus and P. marginellus. Among Photinus species, the presence of male spiral glands-appears to be a reliable indicator of spermatophore production, as spiral glands and spermatophores also occur in P. aquilonius, P. greeni, P. obscurellus, and P. pyralis (unpublished data). In contrast, in P. collustrans, a Florida grassland species, males lack both spiral accessory glands and spermatophores (Wing 1985).

The results of this study indicate that male spermatophores undergo digestion in a specialized gland (SDG) located at the anterior end of the reproductive tract in females of Photinus species within 1-3 days after mating. Such internal diges- tion may simply be a way to dispose of the spermatophore. Alternatively, spermatophore digestion may provide females with nutrients that can be allocated to either reproduction or somatic maintenance. Female P. marginellus mated with rhodamine-dyed males begin to show incorporation of dyed material into developing oocytes within 10 h after the end of copulation. Since rhodamine B forms a stable covalent bond with proteins, it is ur~likely to dissociate once it has bound to spermatophore proteins. The presence of dyed material in female oocytes suggests that spermatophore-derived proteins or amino acids are being incorporated into oocytes during vitellogenesis. This interpretation is also supported by recent work on P. ignitus in which 3H-radiolabelled amino acids were injected into males (J. Rooney and S .M. Lewis, unpub- lished data). Within 48 h after mating, most of the radiolabel transferred in the spermatophore was located in female oocytes. Similar evidence that nutrients derived from male spermatophores are incorporated into female oocytes or soma has been provided by radiolabelling studies in a number of insect taxa (e.g . , Lepidoptera, Boggs and Gilbert 1979; Boggs 198 1 ; Orthoptera, Friedel and Gillott 1977; Bowen et al. 1984; Wedell 1993; Coleoptera, Huignard 1983; Boucher and Huignard 1987).

The time course of spermatophore transfer described here sheds light on the significance of long copulation durations previously observed in several Photinus species (Wing 1985; Lewis and Wang 1991). Copulations last up to 9 h in P. igni- tus, P. macdermotti, and P. aquilonius, and in P. marginel- lus they generally last about 1.5 h (Wing 1985; Lewis and Wang 1991 ; unpublished data). In this study, spermatophore transfer was accomplished within the first 40 min of copula- tion in both P. marginellus and P. ignitus, indicating that pairs maintain genitalic contact for considerably longer than

is required for spermatophore transfer. Prolonged copulation in these spermatophore-producing Photinus species appears to represent copulatory mate-guarding (Alcock 1994). Since copulations generally last longer than the nightly period of male flight and courtship (Lloyd 1966; Wing 1985; Lewis and Wang 1991), females are prevented from mating again that night. In the absence of mate-guarding, the potential for female remating may be high, as firefly pairs are often harassed by rival males during courtship and the early stages of copulation (Papi 1969; Lloyd 1979; Lewis and Wang 1991). In contrast, copulations are generally quite short ( - 1 min) in Photinus collustrans, a firefly species lacking spermatophores; longer copulations only occur when rival males are present (Wing 1984). Selection for male nutrient contributions to females is expected to be accompanied by selection for behaviors that increase paternity assurance. Such copulatory mate-guarding behavior in spermatophore- producing Photinus species may increase the likelihood that a mating male will fertilize oocytes that have received nutrients from his spermatophore.

Boggs (1990) identified some key ecological and physio- logical factors that may influence the relative importance of male-derived nutrients in contributing to female reproduction in insects. These factors include the protein content of the adult diet and the temporal pattern of egg development in females. Oogenesis in insects is generally nutrient-limited, and females may rely on nutrients gathered during either the larval or adult stages (reviewed by Wheeler 1996). Photinus species are not known to feed at all as adults (Williams 1917; Wing 1989; S.M. Lewis, personal observation), so adult dietary protein intake is likely to be negligible in females. In both P. rnarginellus and P. ignitus, females continuously mature oocytes over their adult life-span. The protein resources necessary to sustain continuous vitellogenesis in females of these Photinus spp. need to be acquired either during larval feeding or from male-derived nutrients obtained by adult females during mating. This combination of continuous oocyte development and lack of adult feeding is predicted to strongly select for female utilization of spermatophore- derived nutrients for vitellogenesis (Boggs 1990).

General explanations of patterns of spermatophore occur- rence across related species have been elusive. Within the genus Photinus, spermatophore distribution appears to agree with predictions set forth by Boggs (1990), based on the timing of egg development. Spermatophore presence is also related to marked differences in mating systems and mating behavior among Photinus species. In female P. collustrans, most oocytes are already mature by adult eclosion, so female reproductive output depends primarily on resources acquired during larval feeding (Wing 1985, 1989). Since there is probably little potential for male-derived nutrients to con- tribute to oogenesis in P. collustrans, females are monoga- mous and males lack both spermatophores and copulatory mate-guarding behavior. In contrast, for Photinus species in which males produce spermatophores, females appear to continuously mature eggs during their 1- to 2-week adult life-span. In the three spermatophore-producing species for which mating systems have been described (P. aquilonius, P. macdermotti, and P. marginellus, Wing 1985; Lewis and Wang 1991), females mate with many males over successive nights and males exhibit copulatory mate-guarding behaviour.

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Information on similar aspects of life-history and repro- ductive ecology is likely to be important in developing a general model for spermatophore distribution within other insect groups.

Acknowledgements

E.D.v.d.R. was supported by a grant from the University of New Hampshire's Vice Presidents' Discretionary Fund to M.P. Scott, and part of this research was supported by a grant to S.M.L. from the Massachusetts Natural Heritage and Endangered Species Program. We thank M.P. Scott and C. Walker for facilities and M. Campbell, G. van der Reijden, G. Crossin, and C. Cratsley for field assistance. We are also grateful to J.E. Lloyd, M.P. Scott, S. Wing, and two anony- mous reviewers for helpful comments on the manuscript. This work was completed by E.D.v.d.R. in partial fulfill- ment of the requirements for a Master of Science degree.

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