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Journal of Chemical Ecology

, Volume 44, Issue 9, pp 785–795 | Cite as

Pheromones Regulating Reproduction in Subsocial Beetles: Insights with References to Eusocial Insects

  • Sandra Steiger
  • Johannes Stökl
Review Article

Abstract

Beetles have evolved diverse strategies to cope with environmental challenges. Although parents of the vast majority of beetle species do not take care of their offspring, there are some species, in which parents provide elaborate post-hatching care and remain temporarily associated with their offspring to defend them from competitors or to provision them with food. Usually, socially induced reproductive “control” is a core feature of eusocial societies, but here we highlight that already in small family groups, socially induced reproductive regulation can play a fundamental role. By discussing the family life of burying beetles, we illustrate the mechanisms behind such a reproductive “control” and show that – similar to eusocial insects – pheromones can be an important regulating factor. However, apart from burying beetles, our knowledge of pheromones or other signals mediating reproductive regulation is surprisingly rudimentary for social beetles. More data are required to broaden our currently patchy picture.

Keywords

Family life Fertility signal Parental care Nicrophorus Anti-aphrodisiac Juvenile hormone 

Introduction

When considering the number of species, we have to acknowledge that we are living in a beetle world. The order Coleoptera is by far the most species rich and diverse taxon on earth. Beetles exhibit a wide range of shape and color, utilize a wide spectrum of nutritional resources, from wood to pollen to invertebrates and cadavers, and also evolved a diversity of behavioral strategies. The vast majority of beetle species abandon their eggs after laying them, however, there are some beetles that stay associated to their eggs and protect them from predators, pathogens or competitors (Costa 2006). For example female rove beetles, Eumicrota socia, groom their eggs and egg chamber repeatedly to prevent the invasion of fungal hyphae, which would otherwise drastically diminish hatching success (Ashe 1987). Some beetle parents even engage in post-hatching care and interact with the hatched offspring. Such temporary family living is known, for example, from the darkling beetle Parastizopus amaticeps, a detritivore of the Kalahari and Namib deserts in central and southern Africa. Parenting involves not only protection, but also sustained food provisioning of young (Rasa 1990, 1999). Both parents provide care, thereby showing division of labor, with males digging continually to maintain burrow humidity and females collecting detritus as food source for the developing larvae. There are also beetles that have even evolved a higher degree of sociality, with the ambrosia beetle Austroplatypus incompertus having been described as a eusocial species, due to overlapping generations and a sterile worker caste helping in rearing siblings (Hulcr and Stelinski 2017; Kent and Simpson 1992; Kirkendall et al. 2015). Reproductive division of labor is a hallmark of eusociality and pheromones that signal the presence of a fertile queen have been shown to play a key role in suppressing worker reproduction in some Hymenoptera and termites (Keller and Nonacs 1993; Le Conte and Hefetz 2008; Leonhardt et al. 2016; Matsuura et al. 2010; Van Oystaeyen et al. 2014). Instead of producing their own offspring, workers then focus on the rearing of genetically related siblings. The presence of such queen pheromones has not been revealed for any beetle species yet. However, we have to consider that there can also be situations, in which the reproductive “control” is not directed from mothers to offspring, but also from offspring to parents or siblings or from parents to parents. In general, when offspring is highly dependent on parental resources to survive and grow, both the offspring and parents can benefit if reproduction is temporarily suppressed. Investing resources into the production of additional eggs or embryos might not only severely impact the fitness of the current neonates, as soon as the additional siblings are born, parents might have not the capacity to care for all of them. To avoid a waste of energy and resources, mechanisms must exist that regulate parental reproduction. We know from mammals, including humans, that the interval of the suckling stimulus of newborns can trigger a postnatal infertility (lactational amenorrhea) via an effect on hormones (Dorrington and Gore-Langton 1981; Hamada et al. 1980; Konner and Worthman 1980). However, such offspring caused regulation of fertility has only received little attention in insects. The reason for this shortcoming relies in the strong focus on queen signals in eusocial insects and a neglect of the other social (but not eusocial) insect species. However, from the beetle world, there comes an example of how chemically mediated interactions during family living can regulate reproduction (Engel et al. 2016; Royle 2016). Burying beetles (genus Nicrophorus), which show elaborate and advanced parental care, will be the center of our attention in this review. Our aim is to present the chemical basis of reproductive regulation in the subsocial burying beetles and to put the underlying mechanisms into a more general framework of interactions among family members. Furthermore, we shortly discuss pheromones of other social beetles. We will start with a short overview of the biology of burying beetles and of how pheromones help them to find a mating partner, before we center our attention on reproductive “control” during family living. We have to emphasize that when we speak about pheromonal or reproductive “control”, we do not necessarily imply that the fitness of the receiver is controlled and there is some form of manipulation involved, rather we refer to the proximate level, i.e. the behavior or physiology is affected (please see Peso et al. 2015 for a detailed discussion on this issue).

Family Living on Dead Animals – a Brief Overview the Biology and Behavior of Burying Beetles

Similar to eusocial insects, burying beetle parents meet and interact with their offspring. However, in contrast to the advanced insect societies, burying beetles are characterized by a very short period of family living and siblings do never stay with their parents after eclosion and help to raise the brood. The major factor that has impeded the evolution of eusociality in this genus is the fact that they utilize small vertebrate cadavers, which are of high ephemeral nature, as breeding resource. Burying beetles (approx. 68 described species; Sikes and Venables 2013) belong to the family of Silphidae (carrion beetles) and are well-known for their peculiar behavior of burying small dead vertebrates as a food source for their young (Eggert and Müller 1997; Farbre 1899; Pukowski 1933; Royle and Hopwood 2017; Scott 1998). Attracted by the smell of a decaying carcass (Kalinova et al. 2009), often several burying beetles aggregate (Müller et al. 2007; Schedwill et al. 2018; Trumbo 1992). Intense fights occur between species and within sexes for the exclusive access to the carrion resource. Usually the largest male and female will win the fight and start their reproductive attempt (Hopwood et al. 2014; Otronen 1988; Steiger et al. 2012; Trumbo 1990a). However, depending on carcass size and competition with flies, other constellation are possible and joint breeding of multiple males and females can occur (Eggert and Sakaluk 2000; Scott et al. 2007; Sun et al. 2014; Trumbo 1992). Also on smaller carcasses, defeated individuals rarely abandon the valuable cadaver, but remain in its vicinity. Subordinate males try to sneak matings with the dominant females (Bartlett 1988) and vanquished females take over the role as a brood parasite (Eggert and Müller 2000; Müller et al. 1990a, 2007).

In all burying beetle species studied to date, both sexes are capable of providing care. Adult beetles do not only bury the carcass, but also remove its fur and feathers, shape it into a ball, treat it with antimicrobial anal and oral secretions and manipulate the microbial carrion community (Arce et al. 2012; Cotter et al. 2010; Duarte et al. 2018; Hall et al. 2011; Shukla et al. 2017; Steiger et al. 2011a; Suzuki 2001). Anal secretions of adult burying beetles contain lysozyme-factors, antimicrobial peptides, a range of secondary metabolites and microbes, which all potentially contribute to the chemical preservation of the carcass (Degenkolb et al. 2011; Jacobs et al. 2016; Palmer et al. 2016; Vogel et al. 2017). Eggs are laid asynchronously in the nearby soil (Smiseth et al. 2006) and once the larvae hatch they crawl to the carcass. The larvae are known to beg for food by waving their legs or touching the parents’ mouthpart with their legs (Smiseth et al. 2003; Smiseth and Moore 2004). The adults feed their young with predigested carrion food from mouth to mouth, but as the larvae grow, they increasingly feed on the carcass by themselves (Eggert et al. 1998; Smiseth et al. 2003). Although both males and females are capable of doing all parental tasks, under biparental conditions, females usually engage in offspring provisioning much more frequently than males (Creighton et al. 2014; Head et al. 2012; Walling et al. 2008). Males also abandon the brood earlier than females (Müller et al. 2007; Scott 1994; Scott and Traniello 1990). Females typically stay until the carcass is consumed and the larvae disperse for pupation. Interestingly, the degree of offspring dependence on post-hatching care differs between species, with larvae of some species being able to survive without parental attendance and others not (Capodeanu-Nägler et al. 2016; Jarrett et al. 2017; Trumbo 1992). Such a variation in the phenotypic integration of parental care and offspring development makes burying beetles an exciting model organism for studying the evolution of family life.

How to Spread and Receive Sperm – the Role of Pheromones and Chemical Cues

Male and female burying beetles might find each other because they are attracted to the same cadaver. If a male discovers a carcass alone, he will enhance his chances to reproduce by producing and emitting a volatile sex pheromone to lure females from a distance (Bartlett 1987; Pukowski 1933). However, even so the production of offspring requires a carrion resource, matings also regularly occur in the absence of a carcass. Again, the male sex pheromone makes such sexual encounters possible (Eggert and Müller 1989; Müller and Eggert 1987). Usually males start their daily active period by searching for a carcass, but when unsuccessful they switch to an alternative tactic and engage in pheromone emission towards the end of the activity phase, when female activity is high (Eggert 1992). Females attracted to a non-resource owner will usually mate, as they benefit from receiving fresh sperms (Eggert 1992). Having found a carcass alone, females can use the sperm to fertilize their eggs and raise a brood without a male partner. Although the benefit of a single mating to the male is low, as the females usually also carries sperms from other males, the tactic affords males a large number of mating partners, which increases the chance that they sire some offspring should they themselves fail to find a carcass suitable for reproduction (Eggert 1992).

Until now, the long range pheromone of only two burying beetle species have been identified and confirmed by field studies: N. vespilloides produces ethyl 4-methylheptanoate and geranylacetone, N. humator methyl 4-methyloctanoate (Haberer et al. 2008, 2011, 2017). Chemical analyses revealed that N. humator males also emit a second component, isovaleric acid, but whether it is behaviorally active, has yet to be clarified. Haberer et al. (2017) analyzed the volatiles emitted by males of eight further burying species. The number of components found in the headspace of calling individuals ranged from two to seven, but whether they are all behaviorally active is unknown. Interestingly, methyl or ethyl esters of 4-methylheptanoic acid and 4-methyloctanoic acid are produced by eight of the ten investigated Nicrophorus species, suggesting that the biosynthetic pathway of pheromone production is quite conserved in this genus.

From studies in N. vespilloides, it is known that individuals show large variation in the quantity and ratio of the pheromone components, which impacts their attractiveness under field condition (Chemnitz et al. 2015, 2017b). The amount and ratio emitted is thereby affected by nutritional state, age, body size and parasite load of a beetle. Surprisingly, males are able to produce more of their sex pheromone after than before brood care (Chemnitz et al. 2017a). This result was unexpected as parental care is thought to be costly. However, family life in burying beetles is centered around a highly nutritious diet and feeding from it might boost their sex pheromone production. This benefit might also have promoted the evolution of paternal care in burying beetles. Unfortunately, our knowledge about the variation in ratio and quantity is currently limited to the sex pheromone of N. vespilloides. However, a behavioral study was able to reveal that N. orbicollis females exhibit mate choice based on male’s long range pheromone, thereby preferring larger males (Beeler et al. 2002). Interestingly, the male pheromone has also been shown to foster sexual conflict. On carcasses that are large enough to support more offspring than a single female is able to produce, males often continue to emit their sex pheromone, even though they have already attracted a mate. As the arrival of additional females only enhances the male’s reproductive success, but usually has a negative impact on the fitness of the already present female (the mean number of offspring produced per female is smaller in polygynous association than in monogamous situations), females have evolved the strategy to physically deter pheromone emission by biting and mounting the male (Eggert and Sakaluk 1995; Trumbo and Eggert 1994).

The emission of a long range pheromone does not guarantee that only females are attracted (Chemnitz et al. 2015; Müller and Eggert 1987). Males are known to exploit the sex pheromone of conspecifics to obtain access to females or a carcass. Consequently, to find an appropriate mating partner the sex of an encountered conspecific has to be recognized at a short range as well. Although same sex sexual behavior occasionally occurs in N. vespilloides (Engel et al. 2015), males usually discriminate between the sexes and copulate with females only. Bioassays revealed that cuticular lipids, but not the cuticular hydrocarbon fraction, trigger male mating behavior (Keppner et al. 2017). However, the exact identity of the behavioral active components is still unknown. N. vespilloides is characterized by a complex cuticular pattern comprising more than a hundred components and relative quantity of many components differs between sexes and individuals (Keppner et al. 2017; Steiger et al. 2007). Interestingly, the individual variation is used by males to discriminate between females. Males prefer to mate with novel females over previous mating partners and the discrimination mechanism is based on female cuticular lipids, which are apparently learned during copulations (Steiger et al. 2008). The phenomenon of a decline in the propensity to mate with the same female combined with a renewed sexual interest in new females is known as the Coolidge effect and has been documented in a range of vertebrates and invertebrates. A recent study of Schedwill et al. (2018) was able to confirm that the Coolidge effect can be observed in natural breeding assemblages in N. vespilloides: confronted with several females on a carcass, males did not just mate on every encounter, but tended to avoid re-mating with the most recent mate. Consequently, it is likely that the female chemical cues allow males to spread their sperm more evenly among females. However, we have to emphasize that the Coolidge effect is only short-lived and re-mating of the same female nevertheless occurs during a breeding attempt (Head et al. 2014; Steiger et al. 2008). In fact, in monogamous associations, males are known to re-mate about 170 times from the time of carcass discovery until departure (Engel et al. 2014). At a first glance, this extremely high mating rate seems to be unusual, but similar patterns are known from socially monogamous species of birds, such as the African marsh harriers, Circus ranivorus (Simmons 1990), the white storks, Ciconia ciconia (Tortosa and Redondo 1992), and the northern goshawks, Accipiter gentilis (Birkhead et al. 1987). When arriving on a carcass, burying beetle females usually have sperm in their spermatheca from previous mates. Furthermore, rival males might be around that also attempt to copulate with the resident female. Hence, repeated mating is beneficial to males as it allows them to increase their paternity share (House et al. 2007; Müller and Eggert 1989). However, to females, mating more than twice provides no benefit (House et al. 2008, 2009), but results in costs, as high repeated mating rates have been shown to impair a female’s ability to provide parental care (Head et al. 2014). These differences in costs and benefits give rise to a sexual conflict over mating rate (Royle 2016).

Reproductive “Control” during Family Living

Offspring Affect Female Reproductive State

Females that lay their clutch on limited resources such as dung, carrion or living hosts benefit from carefully assessing the size or quality of the resource and adjust clutch size (Godfray et al. 1991; Hardy et al. 1992; Müller et al. 1990b; Pilson and Rausher 1988). Also parents that defend a territory need to consider its quality when making decisions about the number of offspring to raise (Högstedt 1980). In the case, the offspring rely on parental resources and services, also the parent itself might set limitations (Godfray et al. 1991). In mammals, for example, an upper limit for litter size is usually set by the number of teats (Gilbert 1986). Foraging for food and feeding offspring mouth to mouth does not only cost energy but also time, which inevitably constraints the number of offspring that can be raised. To adequately regulate the number of offspring to the availability of resources, the ideal strategy would be to monitor the number of young and their needs. This would allow the parents to flexibly adjust brood size, i.e. lay new eggs or develop new embryos, when some offspring have died or are already weaned and independent, or kill some offspring in the case the resource quantity has suddenly declined. Vice versa the current offspring would benefit if they influence their mother’s reproductive physiology to keep parental investments directed towards them and not other, future offspring (Mas and Kölliker 2008; Parker et al. 2002; Trivers 1974). Indeed such processes are known to occur in burying beetles: here not only the carcass, but also the presence of offspring impact female reproduction. In general, burying beetle females do not complete the final stages of ovarian development before they have found an acceptable carcass to reproduce (Wilson and Knollenberg 1984). Ovarian maturation is triggered by carrion cues, but the presence of a male is not a prerequisite (Scott and Traniello 1987; Trumbo 1996, 1997; Trumbo and Robinson 2008). Studies have shown that the hatchlings crawling to the carcass then influence the mother’s juvenile hormone III titre (JH III) (Engel et al. 2016; Scott and Panaitof 2004; Trumbo and Robinson 2008). Females caring for young dependent larvae are characterized by very high JH levels and experiments indicate that these high titers temporary suppress females’ fertility and therefore prevent that they continue to produce further offspring (Engel et al. 2016). In fact, the more larvae are present the less likely it is that the mother produces eggs (Fig. 1) and the more likely it is that she cares for the current offspring (Engel et al. 2016; Müller 1987). If the larvae are removed, JH III quantity is significantly lower and mothers resume egg production if carrion is still available (Engel et al. 2016; Müller 1987; Trumbo 1990b; Trumbo and Valletta 2007).
Fig. 1

Comparison of the main factors influencing reproduction in eusocial insects and insects living temporarily in small families. In eusocial insects worker reproduction have been shown to be influenced by pheromones emitted by the queen (mother) and larvae (siblings). In subsocial insects, reproduction of mothers have been shown to be affected by pheromones or other signals produced by their offspring. Mothers in turn affect copulation rate of their male partner

The offspring’s effect on parental reproduction is a mechanism that is expected to be widespread in family living animals. However, if the condition favors the evolution of helpers, i.e. offspring that remain with the family and assist in raising siblings, the situation is different. The mother can continue to lay eggs, as the costs of care are transferred to the helpers. Now, the helpers rely on feedback whether it is still worthwhile to retain from reproduction and consequently, either the mother needs to signal that she is present and still fertile (e.g. fertility signal or queen pheromones) or the helpers need to signal their presence to their siblings (Fig. 1). Research strongly focused on the first mechanism (e.g. Butler et al. 1962; Holman et al. 2013; Oi et al. 2015; Smith and Liebig 2017; Van Oystaeyen et al. 2014; Weil et al. 2009), but there are some studies that indicate that the latter can also play a role. Besides the finding that in the domestic honeybee, queen mandibular pheromones promotes worker sterility, studies also documented that larvae emit (E)-β-ocimene and a blend of ten ethyl and methyl fatty acid esters, which likewise inhibits worker ovaries (Maisonnasse et al. 2010; Traynor et al. 2015). In fact, there is more and more evidence that the larvae contribute to the regulation of worker reproduction in a range of eusocial insects (Fig. 1; Ebie et al. 2015; Heinze et al. 1996; Schultner et al. 2017; Teseo et al. 2013; Ulrich et al. 2016).

In burying beetles, the larval stimulus that leads to the inhibition of female egg laying are currently unknown. Although it is possible that females are somehow able to assess the number of larvae in relation to carcass size, theory predicts that it is more likely that the process involves a signaling process, i.e. larvae signal their need (Godfray 1991; Kilner and Johnstone 1997). The formation of families inevitably leads to conflicts over parental investment (Trivers 1972, 1974), (PI) i.e. “any investment by the parent in an individual offspring that increases the offspring’s survival and reproductive success at the cost of the parent’s ability to invest in other current or future offspring” (Smiseth et al. 2012). Parent-offspring conflict arises as each offspring should demand more PI than parents are selected to provide, because it is more related to itself than to any of its siblings, whereas parents are equally related to all of their offspring. The asymmetries in relatedness generate two sorts of parent-offspring conflicts, (1) interbrood conflict in which offspring enter into conflict with parents over the division of resources between current offspring and its future siblings and (2) intrabrood conflict in which offspring enter into conflict with parents over the division of resources among members of the current brood (Godfray 1995; Kilner and Hinde 2012; Lessels 2012; Parker et al. 2002). Begging signals are thought to have evolved as a mechanism for resolving parent-offspring conflict by communicating information about offspring need or quality. For example in altricial birds, begging signals typically consist of vigorous postural movements, brightly colored gape, and repetitive vocalizations. In insects, begging signals have been less extensively studied (Mas and Kölliker 2008). As chemical communication is the most widespread form of signaling in insects, it is perhaps not surprising that several of the known begging signals in insects seem to be of chemical nature (Mas and Kölliker 2008). In the burrower bug, Sehirus cinctus, for example, mothers exposed to volatiles from nymphs in poor condition provision more food than those exposed to volatiles from well-fed nymphs (Kölliker et al. 2006). Such a solicitation pheromone that affects parental investment might also exist in burying beetles. As already mentioned above, burying beetles larvae show a specialized begging behavior, in which they rear up and wave their legs, thereby touching the parents’ mouthpart (see e.g. Smiseth et al. 2003; Smiseth and Moore 2004). It is also possible that this mechanical signal triggers JH production in mothers and therefore influences her reproductive state. Irrespective of the exact underlying mechanism, the studies document that the presence of offspring has an impact on female reproduction.

Currently, we do not know whether the conflict over PI is resolved closer to the offspring’s or the mother’s optimum in burying beetles. However, both parties definitely benefit from a communication system. As only the mother can produce eggs, the need for regulating the investment into current versus future offspring might be an additional explanation, why females provide more direct care and interact more closely with their offspring than male burying beetles.

A Female Pheromone Controls Male Mating Behavior

Although female burying beetles can raise a brood alone, biparental care is thought to be more common. We know that offspring affect female reproduction, but what about the father? As shortly stated above, males copulate repeatedly with a female when starting a reproductive attempt. However, during the time dependent larvae are present and female egg production is suppressed, neither the male nor the female and offspring would have any benefit from repeated matings. In fact, copulations at this time are likely to be costly for all family members; for the offspring, as copulations can distract the parents from feeding and defending them; for the mother, as copulations have often been shown in other species to have detrimental effects on female survival, for example due to toxic consequences of seminal fluid proteins (e.g. Chapman et al. 1995; Fowler and Partridge 1989; Lung et al. 2002); for the fathers, as they would waste sperm. As expected, detailed monitoring of male mating behavior revealed that males only copulate repeatedly in the beginning of a breeding attempt, but as soon as larvae are present on the carcass, they stop copulating (Engel et al. 2014). In the case, the larvae are removed and the females resume egg laying, the males continue to mate. Does the larvae have a similar effect on their father’s reproductive state as they have on their mother’s? Although this may be possible, the male would be better off, if he was able to directly assess the female’s reproductive state. Vice versa, the female would highly benefit if she could influence male copulations. Indeed, studies have shown that mothers produce a volatile, methyl geranate, during the time they are caring for needy offspring (Engel et al. 2016; Haberer et al. 2010, 2014). The more offspring they are caring for, the more methyl geranate they emit (Engel et al. 2016). The quantity emitted also highly correlates with the quantity of JH III, indicating that methyl geranate reflects hormone titre and therefore a female’s reproductive state (Engel et al. 2016). By injecting a deuterium labelled precursor of JH III, geranyl diphosphate, it became apparent that the hormone and methyl geranate share the same biosynthetic pathway, as breeding females emitted deuterium labelled methyl geranate (Engel et al. 2016). The shared pathway might guarantee the honesty of the signaling system. By means of gas-chromatography coupled with electro-antennographic detection and behavioral assays with synthetic methyl geranate, it was confirmed that male antennae respond to methyl geranate and that the substance is behavioral active: male mating behavior was substantially suppressed by it (Engel et al. 2016). A last experiment verified that the primary function of the pheromone is to deter males from copulating (Fig. 1). On larger carcasses, females are known to tolerate each other and breed side by side, however, they produce significantly less methyl geranate than when breeding with a male partner (Engel et al. 2016).

During the time female egg laying is suppressed, the interest of the male and female regarding mating rate is temporary aligned. Nevertheless, without the release of an honest signal, the male would continue to mate, which might reduce the mother’s ability to provide care (Head et al. 2014) and likely reduces the male’s own engagement in parental care. The pheromonal regulation of mating and parental care behavior is undoubtedly an important component of family life in burying beetles (Royle 2016). Indeed, although the above mentioned experiments used exclusively N. vespilloides as study organism, also other Nicrophorus species produce and emit methyl geranate (S.S. unpublished data). Furthermore, we know from previous studies that methyl geranate (presumably together with cuticular hydrocarbons) allows males to discriminate between their caring female partner and a female intruder to the brood chamber (Haberer et al. 2010; Steiger et al. 2007, 2011b; Steiger and Müller 2010). This recognition mechanism is of high importance, as an intruder tries to take over the carcass for its own reproduction, thereby cannibalizing the resident pair’s offspring (Robertson 1993; Trumbo 1990a, 1990b, 2006).

While queen pheromones are assumed to be honest signals that advertise the presence of a fertile queen and suppress worker reproduction (Keller and Nonacs 1993; Oi et al. 2015; Peso et al. 2015), the burying beetle’s anti-aphrodisiac advertises the presence of a temporary infertile mother and suppresses male reproduction. Although the context is certainly different, both types of pheromones appear to reliably reflect female reproductive state. In burying beetles the reliability is guaranteed due to the physiological linkage with JH III. In the case of queen pheromones, it is not entirely clear and might depend on the type of molecules involved, i.e. CHCs versus other substances. Suggested mechanisms are an intrinsic linkage between pheromone synthesis and oogenesis, a common endocrine control of ovarian development and pheromone production or physiological costs (Holman et al. 2013; Oi et al. 2015). Interestingly, in bumblebees Bombus terrestris, non-reproductive workers have been shown to produce a sterility signal, an example that illustrates that there are also other social species in which pheromones can reflect repressed ovarian or egg laying activity (Amsalem and Hefetz 2010; Amsalem et al. 2009). Here, the chemicals involved are ocetyl esters, with octyl hexadecanoate and octyl oleate as main components. The signal is not directed to any sexual active males; instead, the chemical signal is assumed to function as appeasement signal, reducing aggression of the queen or other workers by informing them that they are “out of the reproductive race” and will refrain from producing any eggs.

What about the Pheromones of Other Social Beetles?

As mentioned above, there is a great diversity in the degree of sociality in beetles, which varies from larval and adult aggregations to biparental families and even eusocial colonies (Costa 2006). However, the chemical communications of these species, especially those that structure family living, are not well studied. In fact, although some sex, aggregation or alarm pheromones have been identified, in none of the species it is known whether and how pheromones regulate the reproductive state of mothers or siblings or control sexual activity of fathers during the period of parental care or family living. Nevertheless, in the following, we briefly discuss some investigated social species.

Many dung beetles (Scarabaeidae: Scarabaeinae) bury a varying number of spheres made from vertebrate dung, on which the larvae are raised. Females of some species stay within the brood chamber until the larvae pupate, tending the larvae and removing mould from the dung spheres (Costa 2006; Simmons and Ridsdill-Smith 2011). Males of several dung beetles species, e.g. in the genus Kheper, produce a sex pheromone in an abdominal gland that is released in a handstand posture similar to that shown by Nicrophorus males. The composition of these pheromones is not fully understood. Although several EAD active compounds were identified from the secretions of Kheper males, experiments testing the attractiveness of these compounds to females in the field failed to produce unambiguous results (Burger 2015). Interestingly, as in burying beetles, some of those putative pheromone components are ethyl and methyl esters of heptanoic acid (Burger 2015). Similar to Nicrophorus females, dung beetles can also sense the presence of eggs and larvae. Females of Copris lunaris only tend brood balls with an egg or larvae present and must therefore be able to detect the presence of the larvae. Most probably this is done using chemical cues, as dung balls impregnated with an extract of brood are also cared for (Klemperer 1982). Although dung beetles are the focus of a wide range of behavioral, ecological and evolutionary studies, there is surprisingly little known about their chemical communication systems (Hanski and Cambefort 1991; Simmons and Ridsdill-Smith 2011).

As mentioned in the beginning, extensive biparental care is also found in the darkling beetle Parastizopus amaticeps (Tenebrionidae). Both the male and the female stay close to their breeding borrow for several weeks to maintain the borrow, ward off conspecific intruders, collect food and to feed the larvae. Adult offspring do not disperse directly after eclosion, but are known to remain in the borrow for approximately two weeks, helping with foraging and feeding younger siblings (Rasa 1999). This prolonged overlap of two generations puts P. amaticpes among the beetle species with the highest degree of sociality. Unfortunately, we know very little on how these family groups are organized. Beetles need to be able to recognize their borrow, breeding partner, adult offspring and conspecific intruders. Most probably CHCs mediate at least some of these recognition processes, which is supported by the fact that the closely related cleptoparasitic beetle Eremostibes opacus mimics the CHC profile of P. amaticpes to enter the breeding borrow of P. amaticpes without hindrance (Geiselhardt et al. 2006). The only pheromone identified in P. amaticpes is the male sex pheromone consisting of 3-methylphenol (52%), ethyl-1,4-benzoquinone (48%), and 3-ethylphenol (2%), which is also produced in aedeagal glands released in a typical handstand posture (Geiselhardt et al. 2008).

The highest degree of sociality in beetles is found in wood-boring bark and ambrosia beetles (Scolytinae and Platypodinae), which not only aggregate in great numbers to attack trees, but also show post-hatching care and family breeding (Kirkendall et al. 2015). Females, and in many cases also males, reside in the gallery system and provide parental care by boring oviposition tunnels, keeping them free of frass, and protecting them against predators and competitors (Kirkendall et al. 1997). In the pine engraver bark beetle, Ips pini, males stay in the gallery system as long as females lay eggs and females lay more eggs with males present (Reid and Roitberg 1994). In ambrosia beetles, parental care additionally includes tending a fungus on which the larvae feed. In Xyleborinus saxesenii, larval and adult offspring of a single foundress have been shown to cooperate in brood care and fungus gardening (Biedermann and Taborsky 2011). As some degree of reproductive division of labour occurs, this species has been described as primitive eusocial (Biedermann and Taborsky 2011). Also in the ambrosia beetle Austroplatypus incompertus, there is evidence that sterile adult female workers are present in the gallery system; colonies can persist for more than 35 years, with single females living up to 4 years (Kirkendall et al. 2015; Kirkendall et al. 1997).

While the aggregation and sex pheromones of bark beetles have been studied in detail for many years (Byers 2004), we have currently no information on the chemical communication between the beetles during breeding and parental care, although there are several interesting aspects, especially concerning the reproductive state of females. For example, does the number of larvae in the gallery system influence female fertility and egg laying? How is the fertility of adult female workers controlled?

Although we have illustrated above how rudimentary our picture of chemical signals in social beetles is, we have to emphasize that there are solitary beetles, which – similar to burying beetles – produce anti-aphrodisiacs to inhibit male mating behaviour. The existence of anti-aphrodisiacs has been demonstrated in two species, the mealworm beetle Tenebrio molitor (Happ 1969) and the rove beetle Aleochara curtula (Schlechter-Helas et al. 2011), but in both cases, the chemical identity of the pheromone has not been determined yet. In both species, it is not the female but the male that produces the anti-aphrodisiac, which is then transferred during copulation to the female partner, rendering them temporary unattractive to other males. Such male transferred anti-aphrodisiacs are also known from other insects, such as flies, bees and butterflies (see references in Malouines 2017; Peso et al. 2015; Thomas 2011). In general, it is thought that they function as paternity protection by eliminating or reducing the chance of sperm competition. Furthermore, we want to briefly highlight that there are also solitary species, in which larval pheromones can have an effect on female egg laying. Aphidophagous ladybirds, for example, avoid ovipositing in patches of aphid prey, where conspecific larvae are present. In the two spot ladybird, Adalia bipunctata, this behavior is mediated by a species-specific oviposition deterring pheromone, a mixture of alkanes, produced by the larvae. The response to the pheromone is adaptive, as larvae are known to cannibalize conspecific eggs (Hemptinne et al. 2001).

Conclusions

Even though family life is diverse and can range from small parent-offspring associations to larger groups of relatives (Kramer and Meunier 2017), chemical communication and reproductive control has almost exclusively studied in eusocial insects, whereas smaller family groups have been neglected (Steiger and Stökl 2017). However, already the evolution of post-hatching care can promote communication processes that regulate the reproductive decisions of family members, such as the parents’ investment into current versus future offspring. In fact, the burying beetle exemplifies that socially induced reproductive regulation is not only an issue of larger social societies, but can also occur in smaller families. We have shown that in those beetles the presence of nutritionally dependent larvae can suppress the fertility of their mother and mothers in turn emit a pheromone that influences the sexual activity of their male partners. However, even though there are many other known examples of family living beetles, we have currently only limited knowledge about their chemical communication systems. We believe that studying them will significantly extend our understanding of reproductive “control” in animal families and societies.

Notes

Acknowledgements

We thank Etya Amsalem and Abraham Hefetz for inviting us to contribute this review. We acknowledge funding provided by the German Research Foundation (DFG) to SS (STE 1874/3-3 and STE 1874/7-1) and to JS (STO 966/2-1), and by the HMWK via the LOEWE Center for Insect Biotechnology and Bioresources.

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Insect BiotechnologyJustus-Liebig-University of GießenGießenGermany
  2. 2.Department of Evolutionary Animal EcologyUniversity of BayreuthBayreuthGermany
  3. 3.Department of Applied EntomologyUniversity of HohenheimStuttgartGermany

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