Spermatophore size in bushcrickets: comparative evidence for nuptial gifts as a sperm protection device.
The adaptive significance of courtship feeding is controversial and has generated considerable discussion (Wickler 1985, 1986; Gwynne 1986a; Sakaluk 1986; Quinn and Sakaluk 1986; Simmons and Parker 1989). Two apparently opposing views exist, although they are not mutually exclusive. The gift may function as a male paternal investment, by increasing the total number or quality of eggs that the female will produce (Downes 1970). Alternatively, the gift may represent a male's mating effort, where the male will trade his gift for fertilizations, thereby increasing his reproductive success by influencing the proportion of eggs that he will fertilize from a given female (Alexander and Borgia 1979).
This controversy of how nuptial gifts affect male reproductive success may partly be the result of a failure to distinguish between the evolutionary origins, selection history, and current maintenance of this behavior (Coddington 1988; Simmons and Parker 1989). Our understanding of the function of courtship feeding derives primarily from experimental studies. Most of these have focused on the maintenance of courtship feeding in terms of paternal investment in bushcrickets (Gwynne 1984a,b, 1986b, 1988a,b, 1990a,b; Gwynne and Simmons 1990; Simmons 1990; Simmons and Bailey 1990; Simmons and Gwynne 1991). In contrast, the effect of sperm competition (i.e., paternity assurance and fertilization success) in relation to nuptial gifts has been largely ignored (Sakaluk 1986; Wedell 1991).
During mating, male bushcrickets provide the female with a spermatophore, which consists of two parts: a sperm-containing ampulla attached to the female's genital opening, and a large sperm-free spermatophylax (the "nuptial" gift), which the female feeds on during and after insemination (Boldyrev 1915). While she is busy eating the spermatophylax, sperm are being transferred from the ampulla to the female's spermatheca. After the female has finished consuming the spermatophylax she will remove and consume the ampulla and whatever sperm that is left. Following mating, the female enters a refractory period during which she starts to lay eggs and is unreceptive to further courtship attempts. In general, the refractory period appears to be induced by substances transferred by the male at mating (Gwynne 1986b; Wedell and Arak 1989), but females seem able to control the duration to some extent (Gwynne 1990; Simmons and Gwynne 1991). The female can mate again at the end of the refractory period.
The function of nuptial gifts has been investigated in only three species of bushcrickets. A paternal investment function was suggested because of positive correlations between measures of female fecundity (number of eggs and/or egg weight) and male nuptial gifts in two species, Requena verticalis (Gwynne 1984a) and an undescribed zaprochiline species (Simmons 1990). This occurs because females utilize nutrients provided in the gift for egg production (Bowen et al. 1984).
However, experimental studies of another bushcricket, the wartbiter Decticus verrucivorus (Wedell 1991), demonstrated a mating-effort function. In this species, larger gifts increased the male's fertilization success, but spermatophylax consumption had no effect on female fecundity, even under situations of food limitation (Wedell and Arak 1989). The male ensures greater protection of the sperm-containing ampulla by providing the female with a larger gift, because it takes the female longer to consume a larger gift, thus increasing the amount of ejaculate that is transferred. This increases the numerical representation of his sperm in the female's spermatheca, which will compete with sperm from other males for fertilization of the female's eggs (Wedell 1991). Additionally, it has been shown that a larger volume of ejaculate increases the duration of the female postmating refractory period and hastens the onset of oviposition (Wedell and Arak 1989). A larger spermatophore will therefore increase the probability of fertilization by directly influencing the outcome of sperm competition but also by increasing the number of eggs laid before a female remates, because it influences the duration of the refractory period.
A Comparative Analysis to the Problem
Experimental studies on single species can usually discern only the maintenance of a function, but current utility does not always imply evolutionary history. Comparative studies on inter-specific variation are frequently helpful in elucidating the selection pressures responsible for various life-history characteristics of organisms, because they examine the general patterns of convergent evolution and may allow inference about evolutionary history (Ridley 1983; Harvey and Pagel 1991). A comparative approach to the function of nuptial gifts is therefore an important complement to the previous experimental studies, because the pattern revealed by this analysis should reflect what has been the more general selection history (and perhaps also the original function of nuptial gifts) in bushcrickets.
In this study, an interspecific comparative analysis of patterns of covariation between spermatophore size (i.e., spermatophylax and ampulla weights) and measures of male and female reproductive variables is performed in an attempt to distinguish between a paternal investment and a mating effort explanation. The two functions of nuptial gifts give rise to two sets of predictions.
Under a ceteris paribus assumption (all other things being equal), the paternal investment function of nuptial gifts implies that female fecundity will be greater as a result of larger gift size (spermatophylax weight). This is because females may utilize nutrients provided in the spermatophylax for egg production. Thus, the paternal investment function predicts, across taxa, a positive correlation between spermatophylax size and fecundity. However, ampulla size is not expected to be correlated with increased fecundity per se. This is because the spermatophore is expected to contain a sufficient quantity of sperm to fertilize all the eggs a female will lay after a mating, regardless of an eventual increase in fecundity caused by gift consumption. Also, because spermatophylax size should be decoupled from the ampulla it can evolve to a size much larger than what is necessary to protect the ejaculate. In R. verticalis, where consumption of male spermatophores increases female fecundity, the spermatophylax is much larger than is necessary to ensure complete sperm transfer (Gwynne 1986b). A correlation between spermatophylax size and ampulla weight is therefore not expected.
The mating-effort function of nuptial gifts predicts that the size of the spermatophore is associated with expenditures in acquiring fertilizations. Males that provide larger spermatophores can increase the probability of fertilization either directly through sperm competition (Wedell 1991) or by increasing the duration of the female's refractory period. This function therefore predicts a positive correlation across taxa between spermatophore size (i.e., spermatophylax and ampulla weight) and the length of the refractory period. A positive correlation between the duration of the refractory period and the number of eggs laid during this period is also expected as a result of the longer refractory period. Furthermore, selection is expected to lead to larger ampulla size, because it is the ejaculate volume that influences the outcome of sperm competition (Wedell 1991) and induces the female refractory period (Gwynne 1986b; Wedell and Arak 1989) as well as stimulates oviposition (Wedell and Arak 1989). This in turn will favor larger spermatophylax size to effectively protect the ampulla, and consequently larger overall spermatophores. However, spermatophylax size need only be large enough to secure complete sperm transfer if functioning as a sperm protection device (Sakaluk 1984; Wedell and Arak 1989; Wedell 1992). Thus, ampulla size is predicted to be positively correlated with spermatophylax size.
MATERIALS AND METHODS
A comparative data set of relevant reproductive and life-history variables, using mean values for each genus, was obtained by direct measurement of 28 species from 19 genera found in Australia and Europe. The reproductive variables measured were, apart from male and female body weight, spermatophylax and ampulla weights for males, and duration of the refractory period, egg weight, and number and mass of eggs laid during the refractory period for females. Males and females were caught in the field, except Ephippiger, which was reared in the laboratory. The specimens were transported back to the lab and kept in individual well-ventilated containers, provided with food and water. Mating took place as soon as possible after collection from the field. Males and females were weighed on a precision balance to the nearest 0.0001 g before and immediately after copulation. Spermatophore size was established by carefully removing the spermatophylax from the female, weighing it, and then presenting it to the female on the end of a blunt needle as she was bending over trying to remove the spermatophore. The female accepted the spermatophylax and immediately started to consume it. The female with the intact ampulla was also weighed following mating to determine ampulla weight. Following mating, females were kept in individual containers and provided with food and water as well as an egg-laying substrate, which was checked for eggs daily. The eggs were removed and weighed. The female refractory period was assessed by placing the female together with stridulating males on each day following mating. A female was classified as being receptive if she showed phonotaxis and attempted to mount a singing male after introduction to the male. Where appropriate, the reproductive variables were logarithmically transformed before analysis to improve normality.
Ideally, comparative analyses should be investigated in a phylogenetic context, because observations on different species are not independent to the extent that they share a common evolutionary history (see Ridley 1983; Felsenstein 1985; Wanntorp et al. 1990; Harvey and Pagel 1991). However, because several of the investigated genera are still undescribed, a cladogram describing the phylogenetic relationships is not available. The analysis was performed at the highest taxonomic level available (i.e., the genus) to minimize the possibility of using nonindependent data points. Mean values were used for each genus, and in cases of multispecies genera, average values for each species were used in the calculations of generic means. Positive correlation between male and female body weight made it necessary to remove the effects of body weight when correlating male and female reproductive variables that were correlated with either male or female size. Where necessary, the residuals of the least-squares regressions of reproductive variables on their respective sex were used. These are referred to as relative measures, are independent of body size, and their use is clearly stated in the text.
Body size ranged between 0.1370 g (Gen. nov. 22) to 2.1744 g (Austrosalomona) for males and 0.2048 g (Gen. nov. 22) to 3.3580 g (Acripeza) for females, and there was a positive correlation between male and female body weight (r = 0.94, N = 19, P |is less than~ 0.001, fig. 1). Spermatophore weight (r = 0.87, N = 19, P |is less than~ 0.001, fig. 2), spermatophylax weight (r = 0.78, N = 16, P |is less than~ 0.001), and ampulla weight (r = 0.91, N = 16, P |is less than~ 0.001) were all positively correlated with male body weight across genera. Egg weight (r = 0.88, N = 19, P |is less than~ 0.001), number of eggs laid during the refractory period (r = 0.57, N = 19, P |is less than~ 0.02), and mass of eggs laid during this period (r = 0.82, N = 19, P |is less than~ 0.001) were all positively correlated with female body weight.
Sexual size dimorphism varied among genera. The most sexually dimorphic genus was Acripeza, with the male on average 3.8 times smaller than the female. Dimorphism, when used in the correlation analyses, was computed as the residual of the regression of male body weight on female body weight. Relatively larger males produced heavier spermatophores relative to their size than smaller males (r = 0.72, P |is less than~ 0.001, N = 19, fig. 3). Regarding the components of the spermatophore, relative spermatophylax size (r = 0.64, N = 16, P |is less than~ 0.01) and relative ampulla size (r = 0.69, N = 16, P |is less than~ 0.01) were both positively correlated with the degree of sexual size dimorphism.
Spermatophore size varied considerably among genera. The largest spermatophore (found in Gen. nov. 12), was around 28% of male body weight, while the smallest (found in Acripeza) represented only about 2% of male body weight. The genus Austrodectes had the largest relative spermatophylax size, representing on average 15% of male body weight. The relatively largest ampulla occured in Caedicia, constituting a mean of 6% of male body weight.
No obvious relationship between female fecundity and male gift size was found. Measures of female reproductive output (i.e., relative egg weight, relative number of eggs laid during the refractory period, and relative mass of eggs laid during this time) were not significantly correlated with either relative spermatophore weight, relative spermatophylax weight, or relative ampulla weight. However, the comparative data are consistent with a mating-effort function. There was a significant positive correlation between refractory period and ampulla weight (r = 0.76, N = 16, P |is less than~ 0.001, fig. 5A), spermatophylax weight (r = 0.78, N = 16, P |is less than~ 0.001, fig. 5B), and total spermatophore weight (r = 0.60, N = 19, P = 0.01, table 2). Spermatophore weight was also positively correlated both with spermatophylax weight (r = 0.96, N = 16, P |is less than~ 0.001) and ampulla weight (r - 0.77, N = 16, P |is less than~ 0.001). More importantly, the relative sizes of the latter two constituent parts of the spermatophore were also correlated with each other (r = 0.59, N = 16, P |is less than~ 0.05), as predicted by the hypothesis that the spermatophylax ensures transfer of the sperm. Finally, the duration of the refractory period was positively correlated across genera with the number of eggs laid during this time (r = 0.50, N = 19, P |is less than~ 0.05) but not with either egg weight (r = 0.26, N = 19, NS) or mass of eggs laid during the refractory period (r = 0.45, N = 19, NS).
The egg-laying rate of female bushcrickets during the refractory period varied between 0.86 to 11.6 eggs per day. The rate of eggs laid was not significantly correlated with either spermatophore size (r = 0.02, N = 19, NS) or duration of the female refractory period (r = 0.33, N = 19, NS).
The results of this comparative analysis support a mating effort rather than a paternal investment function of nuptial gifts as the more general pattern in bushcrickets. Considering all other things being equal, the paternal investment TABULAR DATA OMITTED hypothesis assumes that gift size affects female fecundity, either through increased number of eggs in a clutch, egg size, or production rate of clutches. The mating effort hypothesis, on the other hand, assumes that gift size does not increase the female's gametic mass, but instead affects male fertilization success. The result of the present comparative analysis demonstrates that there is no obvious relationship between gift size and either the number or mass of eggs laid TABULAR DATA OMITTED during the female refractory period. Thus, an increased spermatophylax size does not seem to result in increased fecundity of females across taxa. This contrasts with the view that nuptial gifts in bushcrickets generally represent paternal investment (Gwynne 1983, 1984a, 1986b, 1988a,b, 1990a,b; Gwynne and Simmons 1990; Simmons 1990; Simmons and Bailey 1990). The number and size of eggs that a female lays during her lifetime may be influenced by female quality, longevity, and resources available, without being affected by male nuptial gifts received through repeated matings. Accordingly, oviposition rate may be determined by the female's physiological state (metabolic rate, i.e., female handling time of resources). Egg-laying rate may rather, therefore, be a life-history characteristic of the species. The absence of a positive correlation between female fecundity and male gift size may not necessarily be surprising in itself if differences in female fecundity is largely caused by differences in their life histories. Alternatively, females of species with low reproductive output caused by nutritional constraints may use male contributions resulting in a reproductive output closer to that of other bushcricket species. However, if this were applicable to many of the taxa included in this analysis, it would equally affect the testing of the paternal investment and the mating effort hypotheses.
Variation in spermatophore size seems to be closely associated with fertilization success. Larger spermatophores may increase the duration of the female refractory period. A longer refractory period results in more eggs being laid during this time. Larger gifts increase the length of the refractory period, by way of increasing the amount of ejaculate transferred, but does not increase a female's fecundity. Gift size may conceivably influence female longevity leading to increased female reproductive success, which cannot be controlled for in this study, because lifetime fecundity of all the genera studied are not known. It can be argued, however, that the paternal investment hypothesis should predict a more immediate increase in fecundity, that is, during the female's refractory period, because this is when the investing male has the highest confidence of paternity.
Larger spermatophores seem to lead to longer refractory periods, which will result in a reduction of female mating frequency. However, if egg-laying rate depends on the nutritional state of the female, female lifetime fecundity may be independent of mating frequency. Variation occurs across genera in egg-laying rate during the refractory period. However, neither spermatophore size, including spermatophylax and ampulla size, nor duration of the refractory period has any influence on the egg-laying rate across genera. From the male's perspective a longer refractory period results in higher reproductive success because the female lays more eggs that are fertilized by his sperm.
In the wartbiter, a larger volume of ejaculate, apart from increasing the duration of the refractory period, also hastens the onset of oviposition and increases egg-laying rate during the refractory period in singly mated females (Wedell and Arak 1989). These effects may be caused by hormones passed in the ejaculate. Prostaglandin E2 and other substances produced in male accessory glands induce both vitellogenesis and oviposition of already mature eggs in several insect species (Leahy 1966; Riemann and Thorson 1969; Bryon 1972; Leahy 1973a,b; Loher and Edson 1973; Baumann 1974; Bentur and Mathad 1974; Destephano and Brady 1977; Bentur et al. 1977; Loher 1979; Stanley-Samuelson and Loher 1986; Stanley-Samuelson et al. 1986; Rence et al. 1987). This does not necessarily result in an increased lifetime fecundity of females. In the cricket Gryllus integer, females are liable to suffer from sperm depletion, and need to remate to maintain high hatching success (Sakaluk and Cade 1980). Female benefit from repeated matings may also be related to female choice; females influencing the paternity of their offspring by mating with preferred males thereby diluting the sperm from previous males (Simmons 1986; Zuk 1988). Moreover, females may exercise a postcopulatory mate choice by keeping mating frequency high, that is, promoting sperm competition (Smith 1984).
Because ampulla and spermatophylax size were positively correlated across genera after removing the effect of body size, this may indicate that the spermatophylax functions as a sperm protection device. Larger ampulla size translates to a larger volume of ejaculate, which consists of sperm and accessory substances that influence female refractory period and egg laying. In the wartbiter, sperm mixing seems to occur in the spermatheca (Wedell 1991), and hence there is little evidence for last male sperm precedence. Because large ampulla may contain more sperm, large ampulla size will be advantageous because of sperm competition. In contrast, according to the paternal investment hypothesis, an increase in spermatophore size is thought to be the result of selection for larger spermatophylax size itself, which may affect female fecundity and/or offspring fitness. According to the paternal investment hypothesis spermatophylax size should be decoupled from ampulla size and be free to evolve to a size much larger than that necessary to protect the ejaculate. This has been observed in R. verticalis (Gwynne 1986b). Under the paternal investment hypothesis, a positive correlation is not necessarily expected between ampulla size and gift size for two reasons. First, a larger spermatophylax may result in larger egg size instead of increased egg number (cf. Gwynne 1988a), suggesting there is no need for additional sperm. Second, higher female fecundity does not necessarily require an increased number of sperm to fertilize the additional eggs in the next batch, as the ampulla is expected to contain sufficient amount of sperm to fertilize all the eggs and keep fertility high.
In two butterfly families, it has been suggested that increased ejaculate size is a response to sperm competition, and hence male fertilization success (Svard and Wiklund 1989; Wiklund and Forsberg 1991). Comparative studies within several taxonomic groups have demonstrated a similar pattern with larger sperm-producing capacities as a response to sperm competition (Harcourt et al. 1981; Clutton-Brock et al. 1982; Harvey and Harcourt 1984; Kenagy and Tromulak 1986; Moller 1988a,b; Harvey and May 1989; Moller 1989). Moreover, it has also been demonstrated that a larger ejaculate induces longer female refractory periods in females in at least two butterfly species (Oberhauser 1989; Svard and Wiklund 1991). The same seems also to occur in two species of the bushcricket genus Poecilimon, where larger spermatophore size results in a longer female refractory period (Heller and von Helversen 1991). Males of bushcricket species that are less sexually dimorphic produce heavier spermatophores. Perhaps, large male size is a consequence of selection for larger ampulla size, and therefore larger spermatophore size, because larger ejaculates require a larger protective spermatophylax. It has been shown that ejaculate weight is positively correlated with male size in a number of butterfly species (Rutowski et al. 1983; Svard and Wiklund 1986, 1989; Forsberg and Wiklund 1989; Oberhauser 1989). Given female lifetime fecundity and degree of polyandry, which translates to the degree of sperm competition, males may adjust ejaculate size to increase fertilization success, which requires a larger protective spermatophylax. This in turn leads to an overall large spermatophore size which may affect male size. So, larger male size in bushcrickets may be an evolutionary response to selection for larger ejaculate size required to increase male fertilization success.
The result of this comparative study does not invalidate the present function of courtship feeding as paternal investment in bushcrickets. Males with large investments should have a high confidence of paternity (Werren et al. 1980; Gwynne 1984b), which assumes that the donating males will father the benefitted offspring (Gwynne 1988b). A paternal investment function may have arisen secondarily, once paternity assurance is high. Hence, to males fertilization success can be argued to have priority over investment in individual offspring. According to this scenario, the spermatophylax may primarily have evolved as a sperm protection device; whereas the paternal investment function has evolved secondarily in some species of bushcrickets. Males may also pass specialized nutrients in the spermatophylax that need not result in increased fecundity, but instead enhance offspring survival. The present analysis cannot detect this function, unless it has a major impact on egg weight.
The function of nuptial gifts in bushcrickets has so far been experimentally examined in only three species. The paternal investment view is supported by experimental studies of two of these species (Gwynne 1984a; Simmons 1990), whereas a mating-effort explanation is supported in a third (Wedell 1991). Therefore, taking into account the relative paucity of data, and the results of the comparative analysis presented in this paper, the generality of the paternal investment hypothesis as an explanation for nuptial gift size may require reconsideration.
I thank D. Rentz for his invaluable help with identification and collection of the Australian specimens, E. Nielsen for providing me with working facilities at ANIC during my data collection, A. Martin for facilities at the Zoology Department at Melbourne University where I prepared the manuscript, M. Elgar, S. Nylin, S. Sakaluk, B. Tullberg, P.-O. Wickman, C. Wiklund, and two anonymous referees for criticism and valuable suggestions to the manuscript. This research was supported by grants from the Royal Swedish Academy of Sciences, Lars Hiertas Minne and Wallenbergsstiftelsen.
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|Date:||Aug 1, 1993|
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