The Ins and Outs of Nuptial Gift Giving In Insects

Transcription

1 The Ins and Outs of Nuptial Gift Giving In Insects Emily K. Peachey Colorado State University, Fort Collins, CO ABSTRACT Nuptial gift giving in insects is a valuable tool in mating events and is the means of increased reproductive success in some hexapod species. Gifts given to the female are obtained in three main manners. Most commonly, external glands, salivary secretions, spermatophores or mating plugs, secrete glandular gifts. Next, food items or non-food items may be gathered by the male insect and presented to the female unwrapped or enclosed in a silken package. Lastly, female cannibalization of the male insect can sometimes occur. Two less commonly encountered gifts are: the consumption of a male s waste and pheromonal nuptial gifts. Advantages resulting from the consumption of or the usage of a nuptial gift to the female hexapod include: nutritional nourishment, hydration, increased fecundity rate, protection of freshly deposited eggs. There are other circumstances in which a nuptial gift has an adverse affect on the female. These include reduction of lifespan, changes in oviposition rate, lowered sexual receptivity, and the inability to utilize cryptic mate choice. Benefits of nuptial gift giving in the male insect are: Increased enticement of the female insect toward mating, longer copulation duration, conservation of energy, longer refractory period in female, and the avoidance of sexual conflict. There are several proposed theories of the selection pressures of the evolution of nuptial gifts in insects that will be mentioned in this report. This common behavior of nuptial gift-giving has been passed on throughout the whole hexapod subphylum, beginning with the more primitive of hexapod orders such as the Collembola, moving 1

2 down to the more evolutionary advanced insect orders such as the Diptera and Lepidoptera. Examples of species that participate in this action of giving can be found in almost every insect order in between. INTRODUCTION As a female insect, there are many obstacles that must be overcome when dealing with mate choice and reproduction. Perhaps a solution to these obstacles can be found within the nuptial gift. Nuptial gift giving in insects is an important and interesting behavior involving insect courtship, mating and sexual selection. This behavior, which can also be referred to as nuptial feeding, courtship feeding, or nutritional paternal investment is a behavioral phenomenon that occurs quite regularly throughout the entire insect community. Defining the Nuptial Gift Courtship feeding takes on many different forms depending on the insect species. According to Thornhill (1976a), there are three major types of gifts that the male presents to the female: (1) females may receive nourishment form a glandular product of the male; (2) females received nourishment from food captured or collected by the male; and (3) the male himself may be eaten. These three types of nuptial gifts may be provided to the female before, during or after copulation (Thornhill 1976a). In addition to these common types mentioned, a study conducted by Mullins & Keil (1980) suggest a fourth, less common type of nuptial gift: male waste. Courtship pheromones are another less common type of nuptial gift used in some moth species (Dussourd et al. 1991) 2

3 Glandular Gifts As reviewed by Vahed (1998), glandular gifts can be distributed in four main manners. These are: (1) external glandular secretions including: glands on the male s frons, head, dorsal tergites, tibial spurs, forewings, and also from cephalic and metanotal glands, (2) salivary secretions, (3) the spermatophylax, and (4) spermatophores and substances in the ejaculate. Coleoptera, Zygoptera, Blattodea, and Orthoptera are insects that commonly utilize external glandular secretions as nuptial gifts. This type of feeding can be observed before, during, or after copulation takes place. A variety of functions are exhibited in external glandular feeding including: the protection of eggs, courtship initiation, maximization of ejaculate transfer, and longer mating durations (as reviewed by Vahed 1998). Salivary secretion feeding occurs in species within the orders Diptera and Mecoptera. In the Panorpa species, males will first try to present the female with a gift of edible prey but if unsuccessful they will provide her with a salivary secretion (Vahed 1998). Thornhill (1979) suggests that ingestion of the salivary gift will result in a better ejaculate transfer. He also found that if the male does not provide any sort of gift, the female would most likely not mate with him. A spermatophylax is a large, jellylike substance considered part of the spermatophore. This gift, along with the sperm containing ampulla, remains outside of the female s body while the rest of the spermatophore is inserted in the female. She eats the spermatophylax and the ampulla and when she is finished removes the spermatophore, ending sperm transfer (Vahed 1998). Consumption of the 3

4 spermatophylax is beneficial in some insect species (Gwynne 1984) but can have a harmful effect on others (Vahed 2007; Sakaluk 2006). The spermatophore is a sperm capsule, which does not contain a spermatophylax (Vahed 2007). It is unclear whether or not consumption of the spermatophore provides any nutrient value. Orthoptera, Coleoptera, Diptera, Lepidoptera (Vahed 1998), and Trichoptera (Thornhill 1976a) are all orders of insects in which the male renders a spermatophore as part of ejaculate transfer. Prey Items and Non Food Items Gifts consisting of edible and nonedible food items commonly occur in the families Empididae and Bittacideae from the order Diptera, and in Panorpidae from the order Mecoptera (Vahed 1998). Empidids show a large amount of variation in the items they use for nuptial gifts. In some families, the gifts are wrapped in a silk package but in others, the gift is presented as is. Gifts may consist of the following items: prey that was hunted and captured by the male, dried insect fragments, small pieces of non-edible plant materials, or a seed tufts (Cumming 1994). Many species of Empidids give worthless nuptial gifts and try to trick the female into mating (LaBas and Hockham 2005). Some Empidids will actually present the female with an empty package or even a recycled gift that has been given to another female during copulation and has already been fed on, providing the new female with very little nutritional amenities (Cumming 1994). In the Mecopteran species, the size of nuptial prey presented to female is positively correlated with copulation duration (Thornhill 1976b). Regurgitated crop contents are also a type of nuptial gift that occurs commonly in Drosophila (Chapman et al. 2003). 4

5 Cannibalism Although it is rare, cannibalism is a type of nuptial feeding where a female insect will consume some or all of a male s body before, during or after copulation. This phenomenon has been known to occur in two orthopteran insects (Vahed 1998), sixteen species praying mantis, and twenty-five species of midges (Vahed 1998, Thornhill 1976a). According to Roeder and associates (1960), sexual cannibalism is often a result of being held in captivity and commonly doesn t occur in nature because of the courtship behavior of the male. Interestingly, a mantis can still copulate effectively for days after being decapitated and mating is common among decapitated males (Roeder et al 1960). Waste Mullins and Keil (1980) demonstrated the use of waste products as nuptial gifts in the German cockroach, Blattella germanica. The male German cockroach releases urates from his uricose glands onto the spermatophore. The spermatophore then stays in the female for about a day. After spermatophore removal, tests were performed on the cockroaches and through the use of radiolabeling; uric acids were found incorporated into the oothecae and remained until shortly after eggs hatched. It was suggested that after consumption of the spermatophore, the urates entered into the female by means of the alimentary canal and the genital tract. Mullins and Keil (1980) proposed that the male s urates consumed by the female had a beneficial effect; providing a nitrogen resource to the female and her progeny. DISCUSSION Benefits and Costs Associated With Nuptial Feeding on Female Insect 5

6 There is much debate in the scientific entomological network on whether or not the behavior of courtship feeding is beneficial or detrimental to a female insect. Examples of specific taxa occur in both schools of thought and are presented below. Negative Effects on the Female There are many situations in the insect world where the ingestion of a nuptial gift has a negative effect on a female. These include the reduction in female lifespan, manipulation of oviposition rates, decrease in female sexual receptivity and the prevention of the female to perform cryptic mate choice (Vahed 2007). Reduction of Female Lifespan Within the genus Drosophila, and in few other insects, when a female consumes a nuptial meal of her mates ejaculate it can shorten her lifespan (Chapman et al. 2003). However, this phenomenon rarely occurs in the insect world and is a proposition which is heavily debated (Vahed 2007). Changes Involving Oviposition Rates Another cost associated with nuptial feeding in the female is the manipulation of the rate of oviposition (Vahed 2007). Substances in the males ejaculate cause an increase in oviposition rate but affect a female s ability to produce more eggs at an efficient rate later on in her life with another insect (Vahed 2007). Reduction of Female Sexual Receptivity/Longer Refractory Period Another unfavorable occurrence of courtship feeding is the reduced sexual receptivity of the female insect (Vahed 2007). Sakaluk (2005) suggests that the spermatophylax of the male decorated cricket, Gryllodes sigillatus, contains a substance that prevents or prolongs the female from re-mating. Interestingly, this study found that 6

7 the female G. sigillatus has evolved a type of resistance to the inhibitory substances which are consumed with the spermatophylax. When the spermatophylax was given to a non-gift-giving species, the refractory period was considerably longer than when the spermatophylax was given to the gift-giving species. Inability of Cryptic Mate Choice Although the theory of inability of cryptic mate choice is debated, it is worth mentioning that in some insect species the female s ability to implement cryptic mate choice and interfere with insemination by spermatophore removal is reduced. This is true especially in Ensiferan species (Bateman et al 2001). Positive Effects on Female Benefits related with consumption of nuptial gifts or courtship feedings include nutritional nourishment (Vahed 2007; Vahed 1998), hydration (Ivy et al. 1999), increased fecundity (Thornhill 1976b), reduction in predation due to hunting (Cumming 1994), and protection to freshly deposited eggs (Dussourd et al 1991; Eisner et al 1996) Nutritional Nourishment As previously mentioned, a female insect can obtain nourishment in 3 manners, glandular, prey items and cannibalization of the male (Thornhill 1976a). In the grasshopper Melanoplus sanguinipes, females who had eaten the spermatophylax produced eggs that were considerably larger. Radio-labeled proteins that were found in the spermatophylax were also found in the large developing eggs. These proteins are suggested to provide the female with nutrients that she could not obtain in manners other than the consumption of the nuptial gift (Gwynne 1988). Increased Hydration 7

8 Ivy and colleagues (1999) tested the hypothesis that in the case of the decorated cricket, hydration was obtained via the consumption of the spermatophylax. In their experiments they provided different amounts of water and different numbers of spermatophylexs to the crickets. They found that the females, which were deprived of water, produced less offspring than those who were fed a spermatophylax, which is composed of about 82% water. While number of offspring was increased the consumption of the spermatophylax had no effect on the lifespan of the female. Higher Fecundity Rates Fecundity rate, the ability to produce offspring, is affected by nuptial gift size. Thornhill (1983), studied several aspects of female fecundity rates of a scoripianfly. He found that in this Mecopteran insect, Harpobittacus nigriceps, females which received large blowflies during mating were found to lay significantly more eggs at three hours and at ten hours after mating than unmated females or females receiving small blowflies during mating (Thornhill 1983). Gwynne (1984) found that when working with the bushcricket, Requena verticalis, that a females fecundity rate increased with the number of spermatophores consumed. Also, the sizes of her eggs were larger she increased the number of spermatophores consumed. Lower Predation Risk When a female Empidid is presented with a courtship feeding gift, the likelihood of her encountering a predator is greatly reduced because her mate has done the hunting for her and she does not have to subject herself to the dangerous world of capturing prey (Cumming 1994). Cumming (1994) address how this however; can have a negative influence on the female because she potentially could lose the ability to hunt and will rely 8

9 on the male insect for the much needed nuptial meal. This type of situation can bring about role reversal in courtship activities. Protection to Freshly Deposited Eggs Research conducted in 1988 and 1991 by Dussourd and colleges found that in the male arctiid moth, Utetheisa ornatrix, a pheromone is used. This gift contains alkaloids, which have a protection effect on eggs. Females will choose male who offer this pheromone. Another example of nuptial gifts providing protection to eggs is presented by Eisner and associates (1996). Cantharidin is a toxic chemical that is accumulated through foraging in the beetle species, Neopyrochroa flabellate. This chemical is stored in the male until copulation occurs where it is then transferred to the female with the spermatophore. The cantharidin remains with her during egg formation and is passed on to the freshly laid eggs. Colemegilla maculata, in its larval stage, is a common beetle predator to these eggs. It has been demonstrated that when the eggs are cantharidin-rich, the larvae rarely attack them. Benefits and Costs Associated With Nuptial Feeding on Male Insect Benefits to the Male Insect Many benefits are associated in regards to nuptial feeding in the male insect. This process may be a way in which a male insect can influence the mating performances of a female against her own reproductive interests (Thornhill 1976b; Vahed 1998). Enticing a Female to Copulate Nuptial gifts can help to entice a female to mate with a given male. Many insect won t even consider mating until a gift has been offered. In sagebrush crickets, Cyphoderris strepitans, glandular feeding helps with spermatophore transfer, but does not 9

10 have an effect on the ability of a female to retain the package (Sakaluk and Eggert 1996) Increased Copulation Duration LeBas and Hockham (2005) found that when the dance fly Rhamphomyia sulcata when was presented with a large nuptial gift containing a genuine edible prey item, the copulation duration was increased. If she was presented with a smaller gift or a gift containing an inedible or worthless item, the duration of copulation was decreased. In an experiment by Thornhill (1976b), the copulation durations of a hangingfly: Bittacus apicalis, in the order Mecoptera, were tested. If a female was presented with a large nuptial gift measuring at between mm², copulation durations were between minutes. If the female was presented with a small gift measuring less than 18 mm² the female ended copulation by pulling her abdominal tip away from the abdominal tip of the male. Average duration of copulation was between 5-15 minutes. When she was presented with a distasteful gift, in this case an adult lady beetle, copulation also ended prematurely, after only one minute. As the time of copulation is increased, the amount of sperm transfer is also increased. This is advantageous for the male because it increases the possibility of his paternity (Sakaluk and Eggert 1996) Conservation of Energy Used Usually a cost in energy is associated with the male but in the family Empididae empty silk packages are used to trick the female into mating, without providing her with any type of nutritional nourishment (LeBas et al. 2005). This trickery is advantageous to the males as thy save energy that would be used to hunt and capture an insect (Cumming 1994). Longer Female Refractory Period 10

11 Females in the genera Bittacus and Hylobitacus (scorpionflies) usually mate more than once but if a female receives are large courtship gift she may not be able to mate again for up to two days (Thornhill 1983). Thornhill (1983) watched 60 Harpobittacus nigriceps after mating. Forty of the females re-mated after only 30 minutes. The other twenty had received larger nuptial gifts took two hours to two days to re-mate. This increases the chances that the male with the large gift will be the one to fertilize most of her eggs. Costs to the Male Insect Costs associated with the male insect are few. Roeder and associates (1960) discuss male consumption by the female as a risk. Other risks are increase predation due to hunting, and expenditure of energy for nuptial giving processes (Vahed 1998) Evolution of Nuptial Gifts Several schools of thought exist on the theories on the evolution of the nuptial gift. Kessel (1955) suggests that nuptial gifts are not only to attract the female for copulation but are also a means of avoiding cannibalism or sexual conflict. One theory suggested by Thornhill (1976a) states that a female s tendency to choose mates with a heartier nuptial gift is the selective context in the evolution of all nuptial gift giving insects. Specifically, in hanging flies, he states the feeding of the female by the male during copulation in insects of the family Bittacidae probably evolved by female preference (i.e. intersexual selection) for males willing and capable of increasing their parental investment during reproduction. In bushcrickts, it is suggested that the 11

12 selective context of their elaborate spermatophore (i.e. includes a spermatophylax) system is from both intersexual selection and selection on males to produce offspring with a higher fitness (Gwynne 1984). Another theory of the origin of nuptial gifts is presented by Cumming (1994). He suggests that courtship feeding in Emipidids evolved to decrease predation on the female during hunting events. CONCLUSION Nuptial gift giving in insects is a phenomenon that occurs in the insect world and is a necessary behavior for courtship and mating in some hexapod species. The types of nuptial gifts given are extremely variable form species to species. Additionally, it is unclear if nuptial gifts are, generally speaking, beneficial or detrimental to the male insect. Many examples of each situation can be observed and the effects on the female vary immensely between species. Benefits to the male insect seem to largely outweigh the consequence to the male. It is interesting that functions of nuptial feeding tend to have opposite effects on males as they do females (i.e. when a nuptial gift effects a female negatively, it usually ends up being a beneficial occurrence to the male). Many theories on the selection pressures of the evolution of the nuptial gift exist and they also seem to s change in respect to the insect being studied. Unknown factors are still associated with nuptial gifting in insects causing this behavior to remain an area of active study in the field of entomology. This literature review, in no way, encompasses all or even most oft the published material on nuptial gifts but intends to give a basic understanding of this unique and fascinating animal behavior. 12

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