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User:林偉爵/Sexual cannibalism

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The prevalence of sexual cannibalism gives several species of Latrodectus the common name "black widow spider".

「性食」意指雌性在交配 (mating) 的前、中、或後殺死並取食雄性的行為[1]，這種現象可見於某些無脊椎動物，例如：蛛形綱、螳螂目[2]。目前有四大類不完全互斥的假說嘗試解釋性食的演化，分別為：掠食策略假說[3]、侵略性激增假說[4]、配偶選擇假說[5]、錯誤辨識假說[6]。而性食的發生，一般被認為在兩性的生殖利益上有所衝突[7]。在這些性食的類群當中，雌性通常會在偵測到雄性後不久便發動攻擊，有些雄性則發展出不少行為得以降低被雌性攻擊的機率[8][9]，例如：潛行接近、靜止等。


Prevalence

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性食易見於蛛形綱[10]、端足類[10]、螳螂目[11]，也可見於腹足綱、橈足類[12]、步行蟲科及蠓科[11]。在有雌雄二型性的類群較為常見，極端的雌雄二型性也驅動了性食在蜘蛛中的演化[13]。


Male sexual cannibalism

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雖然雌性通常是性食中發動攻擊的一方，但也有一些逆性食的案例存在，例如：Micaria sociabilis[14][15] 、 Allocosa brasiliensis（英语：Allocosa brasiliensis）[16][17]和 福山魚怪 (Ichthyoxenus fushanensis)[18]。在實驗室的環境下，M. sociabilis的雄性傾向捕食年邁的雌性，其雌雄體型較為接近，且體型越大的雄性越傾向發動性食[15]。A. brasiliensis 的性食則發生在兩個交配季節之間，雄性會在這段非交配期離開藏身處覓食，並且攻擊在這段時期遇到的雌性[17]。福山魚怪在交配季的初期的性食為一般的雌性取食雄性，而到交配季末期則相反，變成雄性取食雌性，且發動性食後，雄性的體積會快速變大並性轉為雌性。這三種逆性食有個共通點，他們都發生於雌性生殖潛能低落的時期，這或許是一種適應性 (adaptive) 的捕食策略。


Proposed explanations

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Female Chinese mantis eats a male copulating with her.

目前有四大類不完全互斥的假說嘗試解釋性食的演化，分別為：掠食策略假說[3]、侵略性激增假說[4]、配偶選擇假說[5]、錯誤辨識假說[6]。

掠食策略假說

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此假說的前提 (assumption) 為性食的發生是因為飢餓、且雌性有能力辨識雄性。此假說認為：

  1. 飢餓的雌性通常處於身體狀況 (body condition) 低落，他們會藉由捕食雄性來提高自身的身體狀況而不是與雄性交配[19]。在螳螂目中，Pseudomantis albofimriata（英语：False garden mantis）雌性的性食可以提高自身的生產力 (fecundity) 和身體狀況 (body condition)[20]。在蛛形綱中，亟需營養來提高卵發育的雌性Dolomedes triton（英语：Six-spotted fishing spider），會選擇取食雄性，即便他們可能是潛在的配偶[21]。食物來源受限的雌性D. triton也比較傾向於發動性食，她們會在交配後取食雄性配偶[21]。發動性食的雌性Argiope keyserlingi可以獲得較多的蛋白質、並產下品質更佳的卵[3]。
  2. 越大型的雄性，其作為食物的能量、營養價值較高，越容易遭性食[22][23]。在Agelenopsis pennsylvanica（英语：Agelenopsis pennsylvanica）和Lycosa tarantula（英语：Lycosa tarantula）的例子中，相較於取食小型的雄性、那些取食較大型雄性的雌蜘蛛，其生產力、卵囊大小、孵化率、以及後代的存活率都會獲得顯著的提升[24][25]，大型雄性作為食物所能提供的養分與能量遠勝於小型雄性，也因此讓雌蜘蛛能孕育更大、更高品質的卵囊[24][26]。
  3. 沒有受精壓力的雌性會傾向吃掉雄性以補充能量。已經交配過的雌性，其性食發生率大於處女雌性[22][27][28]。反之，則受精壓力提高，性食率會下降，例如：當雄性Araneus diadematus的密度低時，雌蜘蛛的性食率也會降低[22][23]。

此假說有個常被討論的問題，在某些雌雄二型性差異極大的種類中，對於雌性而言，一隻蟋蟀可能比都小小的雄性更像是一頓大餐。然而，有研究發現雄性Hogna helluo（英语：Hogna）身上有著蟋蟀所缺乏的的多種蛋白質和脂質[26][29]，取食雄性的雌蜘蛛能獲得比只吃蟋蟀的雌蜘蛛更多的蛋白質[26]。


Aggressive spillover

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The aggressive spillover hypothesis suggests that the more aggressive a female is concerning prey, the more likely the female is to cannibalize a potential mate.[21] The decision of a female to cannibalize a male is not defined by the nutritional value or genetic advantage (courtship dance（英语：courtship dance）s, male aggressiveness, & large body size) of males but instead depends strictly on her aggressive state.[10][21] Aggression of the female is measured by latency (speed) of attack on prey. The faster the speed of attack and consumption of prey, the higher the aggressiveness level.[30] Females displaying aggressive characteristics tend to grow larger than other females and display continuous cannibalistic behavior. Such behavior may drive away potential mates, reducing chances of mating.[31] Aggressive behavior is less common in an environment that is female-biased, because there is more competition to mate with a male. In these female dominated environments, such aggressive behavior comes with the risk of scaring away potential mates.[25][32]

Males of the Pisaura mirabilis species feign death to avoid being cannibalized by a female prior to copulation.[12] When males feign death, their success in reproduction depends on the level of aggressiveness the female displays.[12][33] Research has shown that in the Nephilengys livida species, female aggressiveness had no effect on the likelihood of her cannibalizing a potential mate; male aggressiveness and male-male competition determined which male the female cannibalized. Males with aggressive characteristics were favored and had more chance of mating with a female.[29]

Mate choice

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Nephila（英语：Nephila） sp. eating a conspecific

Females exercise mate choice, rejecting unwanted and unfit males by cannibalizing them.[34][35] Mate choice often correlates size with fitness level; smaller males tend to be less aggressive and display low level of fitness; smaller males are therefore eaten more often because of their undesirable traits.[34] Males perform elaborate courtship dance（英语：courtship dance）s to display fitness and genetic advantage.[36] Female orb-web spiders (Nephilengys livida) tend to cannibalize males displaying less aggressive behavior and mate with males displaying more aggressive behavior, showing a preference for this trait,[29] which, along with large body size that indicates a strong foraging ability, displays high male quality and genetic advantage.[29][37]

Indirect mate choice can be witnessed in fishing spiders, Dolomedes fimbriatus, where females do not discriminate against smaller body size, attacking males of all sizes. Females had lower success rates cannibalizing large males, which managed to escape where smaller males could not.[4] It was shown that males with desirable traits (large body size, high aggression, and long courtship dance（英语：courtship dance）s) had longer copulation duration than males with undesirable traits.[29][37] In A. keyserlingi and Nephila edulis females allow longer copulation duration and a second copulation for smaller males.[38] The gravity hypothesis suggests that some species of spiders may favor smaller body sizes because it enables them to climb up plants more efficiently and find a mate faster.[39] Also smaller males may be favored because they hatch and mature faster, giving them a direct advantage in finding and mating with a female.[40] In Latrodectus revivensis females tend to limit copulation duration for small males and deny them a second copulation, showing preference for larger body size.[37] Another form of mate choice is the genetic bet-hedging（英语：Bet-hedging (biology)） hypothesis in which a female consumes males to prevent them from exploiting her.[41] It is not beneficial for a female exploited by multiple males because it may result in prey theft, reduction in web, and reduced time of foraging.[42] Sexual cannibalism might have promoted the evolution of some behavioral and morphological traits exhibited by spiders today.[37]

Mistaken identity

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The mistaken identity hypothesis suggests that sexual cannibalism occurs when females fail to identify males that try to court.[6] This hypothesis suggests that a cannibalistic female attacks and consumes the male without the knowledge of mate quality. In pre-copulatory sexual cannibalism, mistaken identity can be seen when a female does not allow the male to perform the courtship dance（英语：courtship dance） and engages in attack.[21] There is no conclusive evidence for this hypothesis because scientists struggle to distinguish between mistaken identity and the other hypotheses (aggressive spillover, adaptive foraging, and mate choice).[43]

Male adaptive behaviors

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In some cases, sexual cannibalism may characterize an extreme form of male monogamy, in which the male sacrifices itself to the female. Males may gain reproductive success from being cannibalized by either providing nutrients to the female (indirectly to the offspring), or through enhancing the probability that their sperm is used to fertilize the female's eggs.[44] Although sexual cannibalism is fairly common in spiders, male self-sacrifice has only been reported in six genera of araneoid spiders（英语：Araneoidea）. However, much of the evidence for male complicity in such cannibalistic behavior may be anecdotal, and has not been replicated in experimental and behavioral studies.[45]

Male members of cannibalistic species have adapted different mating tactics as a mechanism for escaping the cannibalistic tendencies of their female counterparts. Current theory suggests antagonistic co-evolution has occurred, where adaptations seen in one sex produce adaptations in the other.[9] Adaptations consist of: courtship displays, opportunistic mating tactics, and mate binding.

Opportunistic mating

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The risk of cannibalism becomes greatly reduced when opportunistic mating is practiced.[9] Opportunistic mating has been characterized in numerous orb-weaving spider species, such as Nephila fenestrata, where the male spider waits until the female is feeding or distracted, and then proceeds with copulation; this greatly reduces the chances of cannibalization. This distraction can be facilitated by the male's presentation of nuptial gifts, where they provide a distracting meal for the female in order to prolong copulation and increase paternity.[9]

Altered sexual approach

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Multiple methods of sexual approaches have evolved in cannibalistic species as a result of sexual cannibalism.[46] The mechanism by which the male approaches the female is imperative for his survival. If the female is unable to detect his presence, the male is less likely to face cannibalization. This is evident in the mantid species, Tenodera aridifolia, where the male alters his approach utilizing the surrounding windy conditions. The male attempts to avoid detection by approaching the female when the wind impairs her ability to hear him.[47] In the praying mantid species, Pseudomantis albofimbrata, the males approach the female either from a "slow mounting from the rear" or a "slow approach from the front" position to remain undetected.[46] The male alters his approach through the utilization of the surrounding windy conditions, and thus the risk of facing cannibalization is reduced.[46]

Mate guarding

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Sexual cannibalism has impaired the ability of the orb-weaving spider, N. fenestrata, to perform mate guarding. If a male successfully mates with a female, he then exhibits mate guarding, inhibiting the female from re-mating, thus ensuring his paternity and eliminating sperm competition.[48] Guarding can refer to the blockage of female genital openings to prevent further insertion of a competing male pedipalps, or physical guarding from potential mates. Guarding can decrease female re-mating by fifty percent.[9] Males who experience genital mutilation can sometimes exhibit the "gloves off" hypothesis which states that a male's body weight and his endurance are inversely proportional. Thus when a male's body weight decreases substantially, his endurance increases as a result, allowing him to guard his female mate with increased efficiency.[49]

Mate binding

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Mate binding refers to a pre-copulatory courtship behavior where the male deposits silk onto the abdomen of the female while simultaneously massaging her in order to reduce her aggressive behavior. This action allows for initial and subsequent copulatory bouts.[8] While both chemical and tactile cues are important factors for reducing cannibalistic behaviors, the latter functions as a resource to calm the female, exhibited in the orb-weaver spider species, Nephila pilipes.[8] Additional hypotheses suggest that male silk contains pheromones which seduce the female into submission. However, silk deposits are not necessary for successful copulation.[8] The primary factor in successful subsequent copulation lies in the tactile communication between the male and female spider that results in female acceptance of the male.[50] The male mounts the posterior portion of the female's abdomen, while rubbing his spinnerets on her abdomen during his attempt at copulation.[8] Mate binding was not necessary for the initiation of copulation in the golden orb-weaving spider, except when the female was resistant to mating. Subsequent copulatory bouts are imperative for the male's ability to copulate due to prolonged sperm transfer, therefore increasing his probability of paternity.[8]

Courtship displays

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Courtship displays in sexually cannibalistic spiders are imperative in order to ensure the female is less aggressive. Additional courtship displays include pre-copulatory dances such as those observed in the Australian redback spider, and vibrant male coloration morphologies which function as female attraction mechanisms, as seen in the peacock spider, Maratus volans.[50] Nuptial gift（英语：Nuptial gift） play a vital role in safe copulation for males in some species. Males present meals to the female to facilitate opportunistic mating while the female is distracted.[9] Subsequent improvements in male adaptive mating success includes web reduction, as seen in the Western black widow, Latrodectus hesperus.[51] Once mating occurs, the males destroy a large portion of the female's web to discourage the female from future mating, thus reducing polyandry, which has been observed in the Australian redback spider, Latrodectus hasselti.[52]

Male-induced cataleptic state

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In some species of spiders, such as Agelenopsis aperta, the male induces a passive state in the female prior to copulation[53] It has been hypothesized that the cause of this "quiescent" state is the male's massaging of the female's abdomen, following male vibratory signals on the web. The female enters a passive state, and the male's risk of facing cannibalism is reduced. This state is most likely induced as a result of a male volatile pheromone.[53] The chemical structure of the pheromone utilized by the male A. aperta is currently unknown; however, physical contact is not necessary for the induced passive state. Eunuch males, or males with partially or fully removed palps, are unable to induce the passive state on females from a distance, but can induce quiescence upon physical contact with the female; this suggests that the pheromone produced is potentially related to sperm production, since the male inserts sperm from his pedipalps, structures which are removed in eunuchs.[53] This adaptation has most likely evolved in response to the overly aggressive nature of female spiders.

Costs and benefits for males

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The physiological impacts of cannibalism on male fitness include his inability to father any offspring if he is unable to mate with a female. There are males in species of arachnids, such as N. plumipes, that sire more offspring if the male is cannibalized after or during mating; copulation is prolonged and sperm transfer is increased.[48] In the species of orb-weaving spider, Argiope arantia, males prefer short copulation duration upon the first palp insertion in order to avoid cannibalism. Upon the second insertion, however, the male remains inserted in the female. The male exhibits a "programmed death" to function as a full-body genital plug. This causes it to become increasingly difficult for the female to remove him from her genital openings, discouraging her from mating with other males.[54] An additional benefit to cannibalization is the idea that a well-fed female is less likely to mate again.[55] If the female has no desire to mate again, the male who has already mated with her has his paternity ensured.

Genital mutilation

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Before or after copulating with females, certain males of spider species in the superfamily Araneoidea become half or full eunuchs with one or both of their pedipalps (male genitals) severed. This behavior is often seen in sexually cannibalistic spiders, causing them to exhibit the "eunuch phenomenon".[49] Due to the chance that they may be eaten during or after copulation, male spiders use genital mutilation to increase their chances of successful mating. The male can increase his chances of paternity if the female's copulatory organs are blocked, which decreases sperm competition and her chances of mating with other males. In one study, females with mating plugs had a 75% less chance of re-mating.[56] Additionally, if a male successfully severs his pedipalp within the female copulatory duct the pedipalp can not only serve as a plug but can continue to release sperm to the female spermathacae, again increasing the male's chances of paternity. This is referred to as "remote copulation".[57] Occasionally (in 12% of cases in a 2012 study on Nephilidae spiders) palp severance is only partial due to copulation interruption by sexual cannibalism. Partial palp severance can result in a successful mating plug but not to the extent of full palp severance.[57] Some males, as in the orb-weaving spider, Argiope arantia, have been found to spontaneously die within fifteen minutes of their second copulation with a female.[54] The male dies while his pedipalps are still intact within the female, as well as still swollen from copulation. In this "programmed death", the male is able to utilize his entire body as a genital plug for the female, causing it to be much more difficult for her to remove him from her copulatory ducts.[54] In other species males voluntarily self-amputate a pedipalp prior to mating and thus the mutilation is not driven by sexual cannibalism. This has been hypothesized to be due to an increased fitness advantage of half or full eunuchs. Upon losing a pedipalp males experience a significant decrease in body weight that provides them with enhanced locomotor abilities and endurance, enabling them to better search for a mate and mate-guard after mating. This is referred to as the "gloves-off" theory.[58]

Male self-sacrifice

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Male reproductive success can be determined by their number of fathered offspring, and monogyny is seen quite often in sexually cannibalistic species. Males are willing to sacrifice themselves, or lose their reproductive organs in order to ensure their paternity from one mating instance.[54][56] Whether it is by spontaneous programmed death, or the male catapulting into the mouth of the female, these self-sacrificing males die in order for prolonged copulation to occur. Males of many of these species cannot replenish sperm stores, therefore they must exhibit these extreme behaviors in order to ensure sperm transfer and fathered offspring during their one and only mating instance. An example of such behavior can be seen in the Australian redback spider. The males of this species "somersault" into the mouths of the female after copulation has occurred, which has been shown to increase paternity by sixty five percent when compared to males that are not cannibalized. A majority of males in this species are likely to die on the search for a mate, so the male must sacrifice himself as an offering if it means prolonged copulation and doubled paternity. In many species, cannibalized males can mate longer, thus having longer sperm transfers.[59]

Monogamy

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Males in these mating systems are generally monogamous, if not bigynous, and have sexually evolved accordingly.[49] Since males of these cannibalistic species have adapted to the extreme mating system, and usually mate only once with a polyandrous female, they are considered monogynous.[60]

Other evolutionary factors

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Sexual dimorphism

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Sexual dimorphism in size has been proposed as an explanation for the widespread nature of sexual cannibalism across distantly related arthropods. Typically, male birds and mammals are larger as they participate in male-male competition.[61] However, in arthropods this size dimorphism ratio is reversed, with females commonly larger than males. Sexual cannibalism may have led to selection for larger, stronger, females in invertebrates.[62] Further research is needed to evaluate the explanation. To date, studies have been done on wolf spiders such as Zyuzicosa (Lycosidae), where the female is much larger than the male.[63]

See also

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References

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