Behavioral Ecology Vol. 10 No. 1: 97-104
© 1999 International Society for Behavioral Ecology
Differential allocation of male-derived nutrients in two lampyrid beetles with contrasting life-history characteristics
Department of Biology, Tufts University, Medford, MA 02155, USA
Address correspondence to J. R. Rooney. E-mailjrooney{at}tufts.edu.
Received 3 March 1998; revised 17 July 1998; accepted 8 August 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Across diverse animal taxa, sperm is transferred from males to females during mating within a spermatophore produced by male accessory glands. In some insects, male spermatophores provide females with nutrients that may be used to increase reproductive output or for somatic maintenance, while in others no such benefits have been detected. Boggs suggested that variation in the current function of spermatophores may be explained by considering ecological and life-history factors. This study examined spermatophore function in Ellychnia corrusca and Photinus ignitus (Coleoptera: Lampyridae), two beetles that exhibit marked differences in adult diet, adult life span, and overwintering stage. During mating, males of both species transfer to females a complex, proteinaceous spermatophore, which is subsequently digested in a specialized sac within the female reproductive tract. Males of each species were injected with 3H-radiolabeled amino acid mixtures and mated with conspecific females. The fate of spermatophore-derived proteins was determined by dissecting females at various times after mating with these radiolabeled males. Females of these two species showed markedly different patterns of incorporation of spermatophorederived nutrients. P. ignitus females incorporated the majority (62%) of spermatophore-derived protein into maturing oocytes within 2 days after mating. In contrast, in E. corrusca a large percentage of radiolabel (46%) appeared in female fat body at 6 days after mating, with a threefold lower allocation to maturing oocytes compared to P. ignitus. These findings support the prediction that short-lived, nonfeeding females are selected to allocate a greater proportion of male-derived nutrients to reproduction, while longer-lived, feeding females are selected to allocate a greater proportion to somatic reserves and maintenance. These results suggest that life-history characteristics may be useful in explaining observed differences in spermatophore function across taxa.
Key words: Ellychnia, firefly, life history, nuptial gifts, paternal investment, Photinus, radiotracer, spermatophore.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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In numerous species, males provide females with nutritional contributions during courtship and copulation. Such nuptial gifts may include captured prey, nutritional substances produced by male accessory glands, or various male body parts (reviewed by Andersson, 1994
; Thornhill,
1976; Thornhill and Alcock,
1983; Zeh and Smith,
1985). Spermatophores, consisting of sperm packaged within a
structure produced by specialized male accessory glands, represent a common
form of nuptial gift transferred during mating in diverse animal taxa
(Mann, 1984). Male spermatophores have
been shown in some insect species to provide nutritional benefits that
increase female reproductive output (egg number or size) or contribute to
female somatic maintenance, while such effects are lacking in other species
(reviewed by Boggs, 1990,
1995;
Gwynne 1997;
Simmons and Parker, 1989;
Vahed, 1998). Boggs
(1990) developed a nutrient budget model
to explain such variation in the relative influence of male-donated nutrients
on female fitness components based on composition of adult diets and timing of
female egg maturation. The examination of spermatophore function in closely
related species with disparate life-history characteristics is likely to
provide insight into selective factors responsible for the maintenance of male
nuptial gifts.
During mating, males of several Photinus firefly species transfer
a complex, protein-rich spermatophore to females (van
der Reijden et al., 1997). After release of sperm bundles into the
female spermatheca for storage, the spermatophore moves into a specialized
compartment within the female reproductive tract, where it subsequently
disintegrates. P. marginellus males fed rhodamine B (a fluorescent,
thiol-reactive dye that covalently binds to proteins) transferred intensely
fluorescent spermatophores to females during mating, and within 58 h female
oocytes became strongly fluorescent. This work suggests that
spermatophore-derived proteins or amino acids may be used by Photinus
females to provision oocytes during vitellogenesis.
In this study we further investigated the current function of spermatophores in two lampyrid beetles, P. ignitus Fall and Ellychnia corrusca LeConte, which exhibit markedly different life histories. Photinus ignitus is a nocturnally active, bioluminescent firefly with short-lived, nonfeeding adults. E. corrusca is a diurnally active, nonluminescent beetle with long-lived, feeding adults that overwinter. We injected males of each species with a 3H-labeled amino acid mixture, allowed them to mate with females, and determined subsequent rates and patterns of radiolabel incorporation into female tissues. We predicted that P. ignitus females would allocate spermatophore-derived proteins primarily to current reproductive output, due to their short adult life expectancy and lack of dietary protein sources for adults. In contrast, E. corrusca females were expected to show greater allocation toward female somatic maintenance and accumulation of metabolic reserves for overwintering.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Ellychnia and Photinus include beetles that are extremely similar morphologically (LeConte, 1881)
,
and McDermott (1964) classified these two
genera in the same subfamily (Lampyrinae), tribe (Photinini), and subtribe
(Photinina). However, these two lampyrid genera exhibit fundamental
differences in several life-history characteristics. P. ignitus
fireflies are nocturnally active and bioluminescent, and are distributed
throughout the northeastern United States (Lloyd,
1966). In eastern Massachusetts adults form discrete breeding
aggregations in open fields from late June to early August. Photinus
beetles overwinter as subterranean larvae, feeding on earthworms and
soft-bodied invertebrate prey (Hess,
1920; McDermott, 1964).
Following adult emergence, males and females of most Photinus species
are capable of mating multiple times, and females continuously mature and
oviposit eggs throughout their 1- to 2-week adult life span
(Buschman, 1977;
Lewis and Monchamp, 1994;
Lewis and Wang, 1991;
van der Reijden et al., 1997; but
see Wing, 1984). Photinus adults
apparently do not feed at all (Williams,
1917; Wing, 1989), and
thus adults rely on reserves stored from larval feeding for both somatic
maintenance and reproduction.
Beetles in the Ellychnia corrusca species complex are common in
forested areas across the eastern United States
(Fender, 1970) and are diurnally active
and nonluminescent. Ellychnia appear to rely on chemical signals for
mate location (Lloyd, 1997). These
beetles overwinter as adults (Williams,
1917), which have been observed feeding on maple sap and flowers
in spring, and on aster and goldenrod in fall (Dillon
and Dillon, 1972; Rooney and Lewis, personal observations).
Both males and females can mate multiple times, and females continuously
mature and oviposit eggs.
P. ignitus males and females were collected at night during their breeding season from June to August 1996 and 1997 in Lincoln, Massachusetts, USA. E. corrusca males and females were collected during the day during their breeding season from March to June 1997 in Lincoln and Belmont, Massachusetts. We examined rates and patterns of incorporation of spermatophore-derived proteins by mating radiolabeled P. ignitus and E. corrusca males to females and dissecting females at various times after mating. Before radiolabel injection, males were paired with females until mating occurred so that males would transfer their existing spermatophore and begin production of a new one. We separated these premating pairs approximately 2 h after the beginning of copulation; for both species, spermatophore transfer occurred within the first 90 min of copulation.
We injected premated males with 10 µCi of 3H-labeled amino
acid mixture (Amersham), and isolated them for 24 h to allow production of a
new spermatophore. Although male spermatophores may also provide females with
substances other than protein (Marshall,
1982), we focused on protein because it is a key nutrient limiting
vitellogenesis (Wheeler, 1996). After 24
h males were placed with a different, field-collected female and allowed to
mate. To determine the location of the transferred label, we interrupted
copulations after approximately 3 h, separated pairs, and dissected females at
various timepoints. P. ignitus females were dissected either
immediately (0 days, n = 6 females), 1 day (n = 4), 2 days
(n = 6), or 4 days (n = 2) after copulation ended;
E. corrusca females were dissected at 0 days (n = 3), 2 days
(n = 4), 4 days (n = 5), or 6 days (n = 2). Under
30x magnification, the following tissue categories were separately
dissected out of each female: spermatophore-digesting gland (SDG),
spermatheca (sperm storage organ), mature oocytes (defined as 
600 µm
diameter), ovaries (including immature oocytes and oviduct), bursa copulatrix,
and all remaining somatic tissue. In a subset of females (n = 11
P. ignitus, n = 14 E. corrusca), fat body was separated from
remaining somatic tissue and counted separately. Each tissue was placed in a
20 ml glass scintillation vial with up to 500 µl of tissue solubilizer
(methanol: hydrochloric acid, 12:1), crushed with a glass rod, and
solubilized overnight at 22°C. Scintillation fluid was added (5 ml
Scintisafe, Fisher) and samples counted with a Packard Tricarb liquid
scintillation counter. We converted measurements of counts per minute (cpm) to
disintegrations per minute (dpm) using a standard 70% counting
efficiency for tritium. No quenching was observed in preliminary tests using
different tissue types or amounts (data not shown).
To compare different female tissues at various timepoints, we converted dpm for each sample to a percentage of the total label transferred to that female; this facilitated comparisons even when the total amount of radiolabel transferred varied among males. Patterns of allocation of male-derived protein were compared between P. ignitus and E. corrusca females using nonparametric Mann-Whitney tests due to heterogenous within-group variances.
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RESULTS |
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E. corrusca male spermatophores were similar to those described previously for Photinus marginellus and P. ignitus (van der Reijden et al., 1997)
,
consisting of a spirally coiled, gelatinous structure transferred to the
female within 30 min after the beginning of copulation. After 1 h of
copulation, sperm bundles had been released into the female spermatheca, and
the remainder of the spermatophore, still largely intact, had moved into the
spermatophore-digesting gland (SDG) (Figure
1). In both E. corrusca and P. ignitus,
spermatophore transfer from injected males resulted in the transfer of a
substantial amount of radiolabel to mated females; total counts in mated
females ranged from 53,000 to 827,000 dpm in 14 E. corrusca females
and from 80,000 to 390,000 dpm in 18 P. ignitus females.
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In P. ignitus females dissected 3 h after the beginnning of copulation (0 days), 74% of the total radiolabel transferred was still associated with the spermatophore located within the female (Figure 2A). The next highest percentage of labeled male protein in P. ignitus females at 0 days was about 11% in mature oocytes located in the lateral or common oviducts. By 1 day after mating, SDG counts declined sharply as the spermatophore disintegrated, and the largest percentage of radiolabel, 44%, was found in female somatic tissue. By 2 days after mating, 62% of the total label transferred appeared in mature oocytes, with female somatic tissue accounting for an additional 27%. All remaining tissues of P. ignitus females, including ovaries, spermatheca (with sperm), and bursa copulatrix, each contained less than 10% of total label across all four time points. The redistribution in P. ignitus females of male-derived label from the SDG, where the spermatophore is initially deposited, to mature oocytes by 2 days after mating is apparent in radiolabel counts expressed as dpm over time after mating (Figure 3).
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In E. corrusca females dissected 3 h after the beginnning of copulation (0 days), 53% of the total radiolabel transferred was present initially in the SDG (Figure 2B), with about 23% in female somatic tissue. As the spermatophore disintegrated within the SDG, a rapid decline in SDG counts was accompanied by a concomitant increase to 64% of radiolabel appearing in female somatic tissue at 4 days (Figure 2B). The majority of this somatic increase was due to increased counts in female fat body (Figure 4), which represented 15%, 37%, and 46% of the total radiolabel in E. corrusca females at 2, 4, and 6 days after mating, respectively. Radiolabel present in E. corrusca mature oocytes reached a maximum of 22% at 6 days after mating, and both the spermatheca and bursa copulatrix contained less than 10% of total label across all four time points.
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Patterns of allocation of spermatophore-derived protein differed markedly between females of the two species. P. ignitus females showed a significantly higher percentage of radiolabeled protein in mature oocytes (mean ± SE = 62 ± 4.3% between 2 days and 4 days after mating, n = 8) compared to the percentage allocated to mature oocytes by E. corrusca females (22 ± 1.2% between 4 days and 6 days after mating, n = 7: Mann-Whitney U test, p =.001). This allocation difference was not due to any differences in female reproductive output, because numbers of mature oocytes were nearly identical between the two species (P. ignitus: 24 ± 3.0 mature oocytes, n = 19 females; E. corrusca: 28 ± 4.3 mature oocytes, n = 14; t = 0.74, p =.47). E. corrusca females, on the other hand, showed significantly greater allocation to fat body at 2 and 4 days after mating (27 ± 4.0%, n = 9 females) compared to P. ignitus females at 1, 2, and 4 days after mating (4 ± 0.3%, n = 8 females; Mann-Whitney U test, p =.001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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This study demonstrates that both P. ignitus and E. corrusca males produce and transfer a protein-rich spermatophore to females during mating, but that females from these two lampyrid species exhibit markedly different allocation patterns of radiolabeled protein derived from these male spermatophores. P. ignitus females allocate spermatophore-derived protein primarily to maturing oocytes, whereas the majority of male-derived protein is allocated to fat body reserves by E. corrusca females.
Three major hypotheses concerning the current adaptive significance of
spermatophores have been proposed (reviewed by Boggs,
1995; Gwynne,
1997; Simmons and Parker,
1989; Thornhill and Alcock,
1983; Vahed,
1998; Wedell,
1993): (1) protecting the male's ejaculate to ensure
successful or increased sperm transfer, (2) providing nutritional
contributions that enhance female fecundity or survival without
increasing male paternity, and (3) providing nutritional contributions that
increase the number or viability of offspring sired by the contributing
male.
Previous studies examining possible nutritional roles for male
spermatophores in insects are summarized in Table
1. These studies fall into two main categories, the first
consisting of studies in which males were fed or injected with specific
radiolabeled compounds and the fate and rate of allocation of male-derived
nutrients within mated females subsequently determined. Many of these
radiotracer studies have demonstrated transfer of substantial amounts of
male-derived nutrients to oocytes, supporting a direct trophic role for male
spermatophores. Similarly high levels of allocation of male-derived protein to
mature oocytes as demonstrated here for P. ignitus females have been
found in the orthopteran Decticus verrucivorus
(Wedell, 1993), although peak
incorporation into oocytes occurs considerably more rapidly in P.
ignitus (2 days versus >12 days). In two cockroaches, Blattella
germanica and Xestoblatta namata, a large percentage (up to
81%) of the urates transferred along with spermatophores are
incorporated into developing oocytes and have been suggested to provide an
energy source during embryogenesis (Mullins and Kiel,
1980; Schal and Bell,
1982).
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Other studies have explored possible nutritional roles for insect
spermatophores by manipulating experimentally either the number or size of
spermatophores received by females and measuring effects on female
reproductive output or longevity (Table
1; also reviewed by Boggs,
1995). For many species, increasing either male spermatophore size
or number results in increased female fecundity (egg number, egg size, or
oviposition rate) or longevity, although a few species show no effect of male
spermatophores on either female fecundity or longevity. Additionally, several
studies have demonstrated an increase in female fecundity with multiple
matings only when females are given low-protein diets
(Table 1). Thus, two lines of evidence
support the idea that spermatophores in certain insects currently function as
a male nutritional contribution that increases availability of protein for
vitellogenesis: (1) radiolabeling studies that demonstrate allocation of
substantial amounts of spermatophorederived protein to oocytes, and (2)
dependence of spermatophore effects on female dietary protein. However, it is
also possible that increased female fecundity with multiple matings or larger
spermatophores may in some cases involve endocrine effects of
fecundity-enhancing substances produced by male accessory glands (reviewed by
Gillott, 1988;
Leopold, 1976).
Few studies have attempted to identify selective forces responsible for the
differences in male spermatophore function observed among species. Boggs
(1990) suggested that differences in adult
diet and temporal patterns of female vitellogenesis may generate differences
in the relative importance of male-derived nutrients to female reproduction.
The present study further suggests that life-history differences may help
explain observed interspecific differences in male spermatophore function. The
difference in allocation of male-derived nutrients observed between these two
lampyrid beetles is consistent with their divergent life histories. Our
findings suggest that in P. ignitus, male spermatophores represent
nutritional contributions that increase female reproductive output, consistent
with Boggs's (1990) prediction of an
increased nutritional role for male spermatophores in species lacking adult
dietary protein sources. P. ignitus adults do not feed, and because
female vitellogenesis is a nutrient-limited process
(Wheeler, 1996), female reproductive
output in the absence of spermatophore-derived nutrients must depend entirely
on resources acquired from larval feeding. Thus, nutrients available in male
spermatophores are likely to be crucial for P. ignitus female
reproduction. In addition, their short 1- to 2-week adult life span may limit
any possible benefit that P. ignitus females could gain from
allocating nutrients to storage for either future maintenance or reproduction.
These life-history features may have been involved in selection for the
ability of P. ignitus females to rapidly divert the majority of
spermatophore-derived proteins to maturing oocytes, thus maximizing current
reproductive output. The transient increase in radiolabel observed in somatic
tissue of P. ignitus females likely represents radiolabeled
polypeptides or amino acids being transported in the hemolymph between the
SDG, fat body, and ovaries; similarly high initial hemolymph counts that
decline over about 24 h have been found in other radiotracer studies
(Boucher and Huignard, 1987;
Friedel and Gillot, 1977;
Huignard, 1983). In P. ignitus
we cannot currently distinguish whether male-derived nutrients are allocated
to eggs fertilized by the donating male or by other males.
In contrast, E. corrusca females allocate the majority of
male-derived proteins to fat body. This allocation may represent long-term
storage, as radiolabel counts remained high in female fat body over at least 6
days after mating. Reduced allocation of male-derived nutrients to
reproduction in E. corrusca females, which feed as adults, compared
to that shown by nonfeeding P. ignitus females agrees with the
prediction of Boggs' (1990) model based on
adult diet, but other life-history characteristics may also contribute to
selection for these differing allocation patterns. Unlike Photinus, E.
corrusca adults live for several months and overwinter in the adult
stage. The large metabolic cost associated with overwintering leads to the
accumulation of extensive fat body reserves before diapause
(Leather et al., 1993). E.
corrusca females collected in the fall have greatly increased fat body
volume compared to females collected in the spring (Rooney J, personal
observation). Adult overwintering, combined with availability of alternative
protien sources in the adult diet, may have resulted in selection for E.
corrusca females to allocate male-derived protein to long-term storage to
support the metabolic demands of overwintering.
Although not addressed in this study, it is also possible that defensive
compounds may be transferred to the female in the male spermatophore. Lampyrid
beetles contain defensive steroidal pyrones called lucibufagins, which are
deterrent to predatory spiders and thrushes (Eisner
et al., 1978, 1997). Several
coleopteran and lepidopteran species are known to transfer defensive compounds
during mating (Eisner et al., 1996;
LaMunyon, 1997;
Sierra et al., 1976). Additional
comparative studies of species with different life histories will provide
further insight into spermatophore evolution.
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ACKNOWLEDGEMENTS |
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We thank Sanjive Qazi and Michelle Gaudette for technical assistance and useful discussion, the Massachusetts Audubon Society and the Minuteman National Historical Society for permission to work on their land, and two anonymous reviewers for their helpful comments. This research was partially supported by a Howard Hughes Undergraduate Research Initiatives Grant.
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