Male dance flies lure females with a dead insect. Not very romantic, you might think, but it certainly does the trick. Hence, such nuptial gifts have evolved in numerous other arthropods...

Courtship in humans often involves presents: diamonds for the girls and showy red sports cars for the boys. Animals do it as well, but on a more modest scale, and of course it is convergent. The so-called nuptial gifts are found in numerous groups of arthropods, especially in the insects and also, much more unusually, in the spiders.

Types and functions of nuptial gifts

Nuptial gifts, which are given to the female by the male, can take various forms. Males might offer food, glandular secretions such as saliva, a spermatophore (a sperm-containing capsule that can be consumed by the female after sperm transfer) or parts of their body (sometimes even all of it, as is best known from the praying mantids). Occasionally, the gift is wrapped in silk. While the distracted female is probing and feeding on it, the male inseminates her.

There is still considerable debate surrounding the function of nuptial gifts in males. Originally, they were assumed to be an example of sexual cooperation and represent paternal investment – the male provides the female with nutrients that she then invests in his offspring. Although some studies have demonstrated positive effects of male gifts on female fecundity, with females producing more or heavier eggs, there is limited support for this paternal investment hypothesis. One problem is that, due to multiple mating by the female, a male cannot be sure that the offspring benefitting from the nutrients in the gift are actually his. In many cases, nuptial gifts seem to serve merely as a leg-up for the male. So they can help to attract a female, enhance his chances of mating or maximise sperm transfer by prolonging copulation (or the duration of spermatophore attachment), thus increasing his chances of paternity. A number of studies have shown that the larger the gift, the more sperm is transferred, which could be a result of active female choice or simply be due to the fact that it takes longer to consume a larger item. Nuptial gifts therefore provide males with an opportunity to manipulate females, and this manipulation can also be more direct. On the one hand, substances in the male’s ejaculate might manipulate the female’s reproductive output or induce a period during which the female is non-receptive. On the other hand, males sometimes re-use gifts (snatching the remains from the female after copulation) or offer worthless inedible ones, which reduces their mating costs. And although the risk of being rejected might be higher and copulation might be shorter with worthless gifts, males might still enjoy an overall benefit by being able to acquire more matings in a certain period of time.

But what about the female perspective? In many cases, females seem to benefit from nuptial gifts; they have been shown to compete for them and to engage in more matings when food is scarce. It remains, however, unclear whether these benefits always outweigh potential costs of mating with a gift-giving male – if they do not, nuptial gifts represent an example of sexual conflict. Particularly if the gift is inedible, there seems to be little direct benefit to the female – so why should she accept a worthless gift? It has been suggested that the female could be led into a sensory trap. If the gift is attractive to the female in a context other than mating (e.g. feeding), she might still accept it even if it has no nutritive value at all. This sensory bias hypothesis, however, remains largely unexplored. Alternatively (or additionally), gifts that are worthless to the female might still be costly to the male and therefore honestly signal a male’s intentions or quality. Furthermore, manipulative males could produce manipulative sons with high mating success. There is evidence that such indirect benefits play a role in at least some species.

Nuptial gifts in insects

The employment of nuptial gifts is widespread in the insects. Several types of gift have independently evolved in various taxa, such as hangingflies (Bittacidae), dance flies (Empididae), bushcrickets and crickets (Orthoptera), scorpionflies (Panorpa), butterflies (Lepidoptera) and beetles (Coleoptera). Only a few examples are given here.

Dance flies

Nuptial gifts in dance flies are manifold, ranging from nutritional prey items to worthless ‘token’ gifts such as leaves or small twigs, and exchanged in an aerial swarm. Often the gifts are wrapped in silk and referred to as nuptial balloons. The silk is produced in salivary glands in the Empidini and in tarsal glands in the Hilarini, which strongly suggests that nuptial balloons have evolved more than once in the Empididae.

Males of the species Empis snoddyi offer empty balloons consisting of numerous silk bubbles, which are accepted by females. It has been suggested that balloon size might indicate male quality, but in mate choice experiments, females surprisingly preferred males with medium-size balloons and large body size rather than males with the largest balloons. At the other end of the spectrum, the gift of E. borealis males is so high in nutritive value that sex roles have become reversed – females compete for males and males then choose a female. In Rhamphomyia sulcata, males offer a nutritious gift as well. However, when the gift was experimentally removed from copulating pairs and replaced with an edible or inedible item, copulation time with an inedible gift was not significantly shorter than with a small genuine gift (but copulation time was still longest with a large genuine gift). Some males with inedible gifts were furthermore able to attract matings with additional females. This suggests that male cheats might be able to invade a species that provides genuine gifts.

Bushcrickets and crickets

In many species of bushcricket (Tettigoniidae), males attach a large spermatophore to the female’s genital opening upon mating. While the sperm is contained in the so-called ampulla, most of the spermatophore consists of a sperm-free gelatinous mass. This nutritious mass (known as the spermatophylax) is consumed by the female,  enhancing female fecundity and offspring fitness in at least some species. The spermatophore is costly to produce, but it ensures sperm transfer and might also represent a paternal investment. In the Australian bushcricket Requena verticalis, the female enters a non-receptive period after mating, the length of which depends on the amount of ejaculate transferred by the male as well as on the female’s nutritional status. This suppression of female receptivity is beneficial to the male (as it increases his chances of paternity), but decreases female lifespan. As the nutritional benefits of the spermatophylax cannot ameliorate this cost, this is an example of sexual conflict. Similarly, the spermatophylax of male Gryllodes sigillatus crickets is likely to represent a sensory trap. It is of very low nutritional value but contains free amino acids that seem to mimic the females’ preferred food.

Some orthopteran nuptial gifts are a little more unusual. In the striped ground cricket (Allonemobius socius), males have a specialised spur on their tibia. During copulation, the female chews off the tip of this spur and ingests a gift primarily consisting of haemolymph. How much haemolymph is transferred depends on the size of the male, with large males offering large gifts. Nuptial gifts can therefore affect the evolution of male body size. In some species (e.g. Hapithus agitator), the female consumes part of the male’s wings during copulation.

Scorpionflies

In scorpionflies (Panorpa), three different mating tactics have been observed. Males may offer a female a prey gift, a salivary secretion or try to obtain matings without a gift. Male Panorpa cognata always offer a gift, but starved males feed extensively on a prey insect themselves before allowing the female to consume the remains. The consumption of male saliva secretions by female P. cognata increases egg production, so this nuptial gift has the potential to function as a paternal investment in offspring.

Butterflies

The males of some butterfly species produce a large spermatophore. In the green-veined white butterfly (Pieris napi), it allows older females to convert their wing muscles into eggs, thus enhancing female fecundity. It is, however, considered unlikely that the male fertilises a significant proportion of the eggs that are supported by his nutrients. Female comma butterflies (Polygonia c-album) also use male-derived nutrients for somatic maintenance and hence manage to increase their reproductive output without suffering reduced longevity.

Beetles

Famously, courtship in fireflies (which are beetles) involves bioluminescent flashes. Less well known is that male Photinus fireflies also offer a spermatophore as a nuptial gift, which enhances female fecundity. At the beginning of the mating season, the duration of the courtship flashes is a reliable indicator of spermatophore size, so females prefer males with longer flashes. Females of the two-spot ladybird beetle (Adalia bipunctata) also consume a spermatophore after mating, but here they do not seem to benefit. Neither fecundity nor longevity is increased, but they lay their eggs faster and become more resistant to re-mating. This suggests that only males gain from spermatophore ingestion. In Neopyrochroa flabellata, males ingest cantharidin (the poison secreted by the Spanish fly Lytta vesicatoria), store it in their reproductive accessory glands and transfer it to the female during copulation. The female then allocates it to her eggs, which makes them relatively invulnerable to predators. Males that have not acquired this substance tend to be rejected by females.

Nuptial gifts in spiders

In comparison to insects, the use of nuptial gifts in spiders is very uncommon. It is best known from the European hunting spider Pisaura mirabilis, but has also been demonstrated in a few other species in the family Pisauridae (Pisaura lama and Perenethis fascigera from Japan, Tinus peregrinus from the USA and Thaumasia argenteonotata from Panama) as well as in three species in the family Trechaleidae (e.g. Paratrechalea ornata). In all these species, the males wrap their gift in silk.

Males of P. mirabilis present their gift to the female during a characteristic visual display. While the female is consuming the gift, the male copulates with her. Males without a nuptial gift have low mating success, and presenting a gift prolongs copulation, thus enhancing male fertilisation success. Also the size of the gift is important, with larger gifts further increasing success. Curiously, P. mirabilis males perform thanatosis, i.e. feign death, when a female is about to terminate copulation. The male collapses into a motionless state, grasping the gift, and is dragged along by the female. Once she takes up feeding, he revives and resumes mating. Thus, thanatosis also increases a male’s chances of completing or lengthening copulation and serves as an adaptive strategy to overcome female resistance to mating. Females, however, do not seem to benefit from the nuptial gift, as neither female fecundity nor offspring size are affected.

It has therefore been suggested that the P. mirabilis gift could represent a sensory trap. Due to the silken casing, the wrapped-up prey resembles the female’s egg sac. After oviposition, females clutch their egg sac and then carry it until the spiderlings hatch. The male might therefore exploit the female’s maternal behaviour. Experiments have shown that the female grabs the gift faster, the brighter and more similar it is to her own egg sac. That the female the eats the gift (which, of course, does not happen in the case of her own egg sac) is likely to be due to her reproductive state. But the silk wrapping might also have other functions, such as making the gift bigger. It furthermore offers the male the chance of deception – as the female cannot immediately see what is inside the casing, males sometimes wrap worthless items, such as plant parts or empty arthropod exoskeletons. Although males presenting such worthless gifts do not attract fewer matings than those males offering edible items, females that receive worthless gifts terminate copulations faster. And since the time of copulation affects sperm transfer and hence male fertilisation success, there is a cost to male deception. There is, however, also a cost to gift production in the first place, as the male has to produce the silk and spend time wrapping the item. Males in poor condition are less able to construct gifts, so gift construction could honestly signal male condition and therefore be important in female choice.