Ultimate sacrifice or opportunistic foraging?

Abstract

The discovery of rare cases of males cannibalising females sheds new light on the selective forces behind sexual cannibalism in the animal kingdom.

Cannibalism is widespread in the animal kingdom and often involves the consumption of offspring by parents or other adults when food is in short supply. The subset of sexual cannibalism is also very common but largely confined to invertebrates; only a small number of vertebrates including some snakes feed on the other sex. Sexual cannibalism, whereby females eat males after copulation, does make sense from an evolutionary point of view and is even sustained by natural selection to give offspring a better start into life by providing their mother with additional resources.

Cases where males eat females during copulation are much rarer because such behaviour would seem to make no sense evolutionarily. However, sexual cannibalism by males has recently been observed in a snake species, shedding new light on the phenomenon and raising the question of what selective forces are at play, if indeed any.

Cases where males eat females during copulation are much rarer because such behaviour would seem to make no sense evolutionarily.

Male cannibalism

The species concerned, Malpolon monspessulanus known colloquially as the Montpellier snake, is indigenous to the south of France rather than a tropical country with a far larger snake population (Fig 1). A study based on observations submitted to a community reporting system described three instances of adult male snakes feeding on adult females, with suggestions of possible evolutionary drivers (Glaudas & Fuento, 2022). “At first, we thought it seems counterintuitive that a male would eat potential mating partners, because this male would lose the opportunity to mate with her and produce more offspring” commented Xavier Glaudas, an honorary researcher at the University of the Witwatersrand, South Africa, and currently affiliated with the University of Sao Paulo, Brazil.

Figure 1. The Montpellier snake Malpolon monspessulanus is a rare case of male cannibalism on females. Laurent Rouschmeyer/Wikimedia Commons/CC BY 3.0.

The authors then conducted a review of the literature and found few examples of males cannibalising females among vertebrates in particular, even away from sexual contact. “We failed to find a single record of it for mammals, amphibians and reptiles in reviews written by Polis, an expert on the topic, who is now deceased I believe. We were able to dig out a few observations in mammal species, polar bears and leopards, and to find a few cases in another snake species, the King Cobra,” said Glaudas.

He noted that cannibalism occurs more widely among animals that have a broad diet, on the basis that a narrow specific diet is unlikely to include members of the same species. The Montpellier snakes are opportunistic predators and aggressive feeders, and the first possible explanation for their male sexual cannibalism could be just a case of a hungry individual entering predatory mode. The second idea, somewhat related, is that cannibalism occurs when the more typical prey is in short apply and males take an opportunity to feed on one of their own as it were. A key point is that male Montpellier snakes are larger than females. When sexual cannibalism occurs, it is almost invariably the smaller sex that ends up being consumed and so in this case females would be vulnerable to opportunistic predation.

… cannibalism occurs more widely among animals that have a broad diet, on the basis that a narrow specific diet is unlikely to include members of the same species.

Glaudas's third hypothesis is that cannibalism removes a competitor for the same ecological niche. There are plenty of examples of animals acting to deter members of their own species competing directly for resources, with some such as robins being notably territorial. But it is unlikely that sexual cannibalism by males would be selected purely on an ecological basis.

More likely, according to Bryan Maritz from the University of the Western Cape, South Africa, is that sexual cannibalism by males provides nutritional benefits that outweigh the loss of available females, especially in snakes, which eat rarely but in large doses. “Foraging in snakes is a complicated game,” he noted. “Many snakes, and nearly all the cannibal species, are generalised predators that are likely to respond to a range of different feeding stimuli, so the chance of a mistake being made is not zero. Moreover, the argument for natural selection weeding out such behaviours requires that those behaviours take place sufficiently often for the negative impacts of cannibalism to have impacts on the fitness of cannibals. I'm not convinced that those negative impacts are very large, so as long as it's happening at relatively low frequencies it might not be a huge issue. The same argument holds for sexual cannibalism, and I think that the costs of cannibalism in those cases can be drastically reduced if, for example, that female wasn't reproductively receptive at the time.”

Maritz welcomed the Glaudas study as a valuable addition to the field. “It is a significant finding. Mostly, it shows that cannibalism in all snakes is not the same. The evolutionary advantages and disadvantages of males eating males, versus males eating females are very different,” he commented. In fact, the findings build on observations of cobras a few years earlier by Maritz himself and colleagues (Maritz et al, 2019), who described how cannibalism among many snakes was more common than had been thought. “Our main point is that African cobras eat members of their own species far more regularly than anyone really expected,” Maritz said. “Snakes make up a huge part of their diets, but cannibalism was very common. We hypothesised from a small sample size that it arose as an extension of male‐male combat, in which males are known to bite each other, and has been selected for because of the huge energetic gains that are received from eating a large meal. Snakes fit inside other snakes really well, so they are often relatively large meals.”

Size matters

Similar considerations hold for spiders, which frequently engage in cannibalism when in close proximity, which is one reason they cannot be successfully farmed for, say, silk production. While female spiders are often larger and therefore the cannibals, this is not always the case and sometimes male spiders indulge too. This has been observed in the Micaria sociabilis spider species (Sentenská & Pekár, 2014) and Allocosa brasiliensis (Aisenberg et al, 2011) where males and females are comparable in size, and so, larger individuals of either sex may occasionally feed on smaller ones of the other.

These may be examples of adaptive foraging, which is one explanation for sexual cannibalism, whereby individuals prey on what is available. In a laboratory experiment on M. sociabilis, males were found to prefer eating older females with less reproductive potential at times when food is limited, a clear example of adaptive foraging where predation is balanced against other considerations such as reproduction (Aisenberg et al, 2009). A similar argument applies to the habit of A. brasiliensis males being cannibalistic in between mating seasons, during which females they encounter are less likely to have reproductive value.

The much more widespread phenomenon of sexual cannibalism by females has been definitely subjected to strong selection pressure in many animals. It also provides plenty of examples of sexual selection whereby males and females are subject to different and sometimes opposing evolutionary forces. This, in some cases, leads to a selective arms race between males and females of the same species. In other cases, sexual cannibalism has led to more symbiotic relationships between the sexes where the males appear to collude in their death to maximise the survival prospects for their offspring.

In other cases, sexual cannibalism has led to more symbiotic relationships between the sexes where the males appear to collude in their death to maximise the survival prospects for their offspring.

A convenient snack

Sexual cannibalism is a subcategory of semelparous behaviour where animals die after mating. It applies to plants that die after reproducing, as well as animals, such as salmon, where both sexes die after spawning, driven presumably by selective pressure to save precious food in the rivers for their offspring. The more special case of sexual cannibalism by females is also common among insects, arachnids, amphipods and to a lesser extent gastropods and copepods. Amphipoda is an order of malacostracan crustaceans comprising around 10,000 species with laterally compressed bodies ranging in size from 1 to 340 mm long that mostly scavenge for food. Gastropods are a large taxonomic class including snails and slugs from saltwater, freshwater and land. Copepods (“oar‐feet”) are small crustaceans found in almost all freshwater and saltwater habitats, including plankton and benthic species living on the ocean floor. This highlights the extent of sexual cannibalism, with the one common factor of sexual size dimorphism (SSD). Such imbalance may encourage sexual cannibalism usually by females and drive the selection for it.

There are different degrees of sexual cannibalism with some appearing to be cases of adaptive foraging, while in other cases the males participate actively in the process, sacrificing their own lives for the greater good of the species. The praying mantid, which could easily be called the preying mantid, is a celebrated example of a species where females cannibalise males routinely during mating to increase their rate of reproduction (Barry et al, 2008; Fig 2). That study was one of the first to position sexual cannibalism as a direct extension of adaptive foraging. It was also one of the first to discuss an example of sexual cannibalism in a species that was only moderately sexually dimorphic for size, in this case, the males being not much smaller than the females.

Figure 2. The praying mantis or “preying mantis” Pseudomantis albofimbriata is one of the best‐known examples of female sexual cannibalism. Graham Wise/Wikimedia Commons/CC BY 2.0.

The authors note that until then, most studies of female sexual cannibalism had focused on highly dimorphic spider species where the males were so much smaller than the females that they made little contribution to female body mass upon consumption. They argue that in the case of the praying mantid, Pseudomantis albofimbriata, with only moderate sexual size dimorphism and therefore relatively large males, cannibalistic females gained a substantial nutritional advantage from sexual cannibalism.

While the degree to which this is selective was speculative, the study found clear evidence that the prevalence of sexual cannibalism was affected by the physical condition of the females. Those in poor condition were more likely to consume their mates as a way of gaining strength and therefore fecundity than females in good condition. Additional analysis refuted the relevance of other hypotheses for sexual cannibalism, providing clear evidence that foraging strategy is behind the maintenance of sexual cannibalism in this species.

… the study found clear evidence that the prevalence of sexual cannibalism was affected by the physical condition of the females.

There are at least two other hypotheses to explain female sexual cannibalism beyond the adaptive foraging strategy. These are the aggressive spillover hypothesis, and the sexual selection hypothesis, which tends to pull in opposite directions. The first suggests that females consume males partly because they are convenient sources of food as an extension of a generally robust approach to preying, which is somewhat related to adaptive foraging, although more indiscriminate. The sexual selection hypothesis posits that females tend to select males for eating that are smaller and appear less fit, so as to minimise the impact on the population of genetically more suitable males. In the case of this praying mantid, it appears that females go for fit males, and more so when they are in need of sustenance themselves, which seems to rule out sexual selection and points towards optimising food intake at this critical time.

Selective forces at work

The question then arises of what selective pressures operate on those animals, including many spiders when females are far larger than males, such that the nutritional benefits are smaller. In these cases, selective forces revolve around reproductive fitness and fecundity. In spiders this has been studied in the context of mating plugs, gelatinous secretions deposited, usually by males, into female genital tracts, that resist further intrusions and therefore reproduction after the sexual act. In a number of vertebrate and invertebrate species, such plugs play a key role in sperm competition between males to maximise chances that the target female gives birth to their own offspring exclusively. Although females can expel the plugs at some point, the male's sperm gains a window of opportunity to fertilise eggs before sperm from other males can get in.

Male Australian redback spiders are renowned for performing somersaults directly into the mouths of females after mating, which increases the number of offspring produced.

The plugs are inserted most often by males, but in some spiders, it is a cooperative effort by both partners, and in a few cases is performed just by females and can interplay with sexual cannibalism. A recent study investigated this behaviour in the orb spider Leucauge argyra because, unusually, it is the females that exclusively produce the plugs that either partially or totally block the entrances to their insemination ducts (Hernandez Duran & Barrantes, 2022). It also confirmed that smaller males were more likely to be attacked around the time of mating, suggesting it may be associated with fitness as assessed by the females. The study shed further light on mechanisms associated with mate plug formation in this case when it is under female control, building on an earlier publication (Hernández et al, 2018), which found females of two geographically separated groups of this species to behave differently, as Linda Hernández Duran from the James Cook University, Cairns, Australia, and lead author on the paper explained: “The species that we studied is quite particular because, in previous studies, females from Costa Rica never attacked males, but in the species from Colombia, females started attacking males when the males reduced the number of hematodochal expansions, movement related to sperm transference.” In other words, females started cannibalising males that appeared less fit.

The ultimate sacrifice

There are also cases of sexual cannibalism where males actively participate in, or encourage, female sexual cannibalism, in seemingly complete evolutionary convergence between the sexes. Male Australian redback spiders are renowned for performing somersaults directly into the mouths of females after mating, which increases the number of offspring produced. Such self‐sacrificial mating behaviour, also observed in brown widow spiders, tends to occur among species that are highly venomous and monogamous, where the males appear to focus on one major mating event in their life with a single female.

However, natural selection should favour the evolution of males that adopt strategies to prolong their mating life and that has also been observed in the case of redbacks: Some males avoid immediate consumption by immature females that are not yet able to consume their partners (Biaggio et al, 2016). The study showed that males can increase their reproductive success by copulating with young females after piercing their exoskeleton to access their newly developed sperm storage organs. Females then retain sperm during their final moult and produce offspring. Although this may result in smaller broods than mating with mature adults, the male usually lives to mate again and so maximises numbers of his own offspring. Such mating with immature females is quite common among invertebrates and may well be a widespread adaptive behaviour, admittedly not always associated with sexual cannibalism.

There are other strategies that males have evolved among invertebrate species to reduce the risk of being cannibalised. This includes the distraction of females in various ways and, as an extension of that, the presentation of nuptial gifts, not in the hope of return generosity but to give them something else to feed on. This is the case with nursery web spiders (Pisaura mirabilis; Fig 3) where males sometimes present insects to females during mating, at least partly to reduce the risk of being consumed in the process. One study (Toft & Albo, 2016) found that males mating without gifts were more likely to end up being cannibalised. It also found that the presentation of gifts was reinforced by other selective strategies, such as the development of strong forelegs to guide the female body towards the gift and away from itself. Again, such presentation of nuptial gifts is quite common among vertebrates and invertebrates, driven by sexual convergence, since it is in the interests of both sexes for females to have a nutritious meal to enhance the production of offspring. The mechanism then seems to have become more defensive for males among species where the females are larger.

Figure 3. The male nursery spider Pisaura mirabilis present “wedding gifts” to distract the female spide while mating. Anna N Chapman/Wikimedia Commons/CC0 1.0.

Sexual cannibalism is not a new discovery and has been chronicled and studied for many years, but the recent observations of male cannibalism and further research on the evolutionary drivers have shed new light on this behaviour and their selective advantages. Beyond, it also gives more insights into the eternal battle between the sexes during their coevolution.

EMBO reports (2023) 24: e56764