Intraspecific female brood parasitism in the dung beetle Onthophagus taurus

Abstract.  1. Brood parasitism occurs when individuals parasitise each others' investment into parental care, and has been documented primarily as an interspecific interaction. Intraspecific brood parasitism, in contrast, is often difficult to detect and quantify, and evidence for it is comparatively scarce. The present study documents the occurrence of intraspecific brood parasitism by females of the tunnelling dung beetle Onthophagus taurus , and investigates the contributions of two variables to the propensity of female brood parasitism: female body size and dung desiccation rate.
2. Female O. taurus were found to routinely utilise brood balls made by conspecific females as food provisions for their own offspring.
3. Contrary to expectations, large and small females did not differ in the likelihood of engaging in brood-parasitic behaviour.
4. Dung desiccation rate appeared to influence likelihood of brood parasitism. Females that were given access to rapidly drying dung were significantly more likely to detect and utilise brood balls produced by conspecific females.
5. While interspecific brood parasitism has been documented in dung beetles before, the present study is among the first to present evidence for intraspecific brood parasitism as an alternative reproductive tactic of female dung beetles. Results are discussed in the context of the evolutionary ecology of onthophagine beetles.     

Maternal and paternal effects on offspring phenotype in the dung beetle Onthophagus taurus

Abstract.— Parents often have important influences on the development of traits in their offspring. One mechanism by which parents are able to influence offspring phenotype is through the level of care they provide. In onthophagine dung beetles, parents typically provision their offspring by packing dung fragments into a brood mass. Onthophagus taurus males can be separated into two discrete morphs: Large, "major" males have head horns, whereas "minor" males are hornless. Here we show that a switch in parental provisioning strategies adopted by males coincides with the switch in male morphology. Male provisioning results in the production of heavier brood masses than females will produce alone. However, unlike females in which the level of provisioning increases with body size in a continuous manner, the level of provisioning provided by males represents an "all-or-none" tactic with all major males providing a fixed level of provisioning irrespective of their body size. Offspring size is determined largely by the quantity of dung provided to the developing larvae so that paternal and maternal provisioning affects the body size and horn size of offspring produced. The levels of provisioning by individual parents are significantly repeatable, suggesting paternal and maternal effects as candidate indirect genetic effects in the evolution of horn size in the genus Onthophagus .     

Game theoretic model of brood parasitism in a dung beetle Onthophagus taurus

We present a game theoretic model of brood parasitism in the dung beetle Onthophagus taurus. Female O. taurus engage in brood parasitism when they attack a brood ball made by another female, destroy the existing egg and place one of their own eggs to develop within the existing dung ball. Brood parasitism is more costly than other forms of kleptoparasitism because an individual loses the total investment in an offspring. In this paper, we outline the behaviors involved in brood ball production and provide time estimates of those behaviors. The model is then used to predict when it is beneficial to steal the brood ball created by another female and when it is beneficial for a female to create her own. We also investigate how long a female should guard her eggs.     

Experimental evidence for the role of sexual selection in the evolution of cuticular hydrocarbons in the dung beetle,Onthophagus taurus

A role for sexual selection in the evolution of insect cuticular hydrocarbons (CHCs) is suggested by observations of selection acting on male CHCs during female mate choice. However, evidence that CHCs evolve in response to sexual selection is generally lacking, and there is a need to extend our understanding beyond well‐studied taxa. Experimental evolution offers a powerful approach to investigate the effect of sexual selection on the evolution of insect CHCs. We conducted such an experiment using the dung beetle, Onthophagus taurus. After six, 12 and 21 generations of experimental evolution, we measured the CHCs of beetles from three populations subject to sexual selection and three populations within which sexual selection had been removed via enforced monogamy. We found that the male CHC profile responded to the experimental removal of sexual selection. Conversely, the CHC profile of females responded to the presence of sexual selection but not to its removal. These results show that sexual selection can be an important mechanism affecting the evolution of insect CHCs and that male and female CHCs can evolve independently.     

Dung pad residence time covaries with male morphology in the dung beetle Onthophagus taurus

1. The immigration and emigration behaviours of Onthophagus taurus were investigated in a combination of field and laboratory experiments to examine patterns of dispersal in this species. 2. On average, the mean proportion of major males immigrating to baited pitfall traps decreased significantly with time. In contrast, the mean proportion of minor males and females did not change with time. 3. The time taken to emigrate from a dung pad differed significantly among major males, minor males, and females. This difference arose because major males spent a significantly shorter period of time residing within the dung pad. On average, more than 50% of major males had emigrated from the dung pads after 30 h, some 4 h earlier than minor males and females. 4. When the effects of body size were controlled, major males with longer horns were shown to have longer wings. Because major males spend more time in flight, longer wings may be an adaptation to more frequent dispersal. Alternatively, longer wings in major males may compensate for the production of aerodynamically costly horns.     

No evidence for condition-dependent expression of male genitalia in the dung beetle Onthophagus taurus

We examine the condition-dependence of male genitalia in the dung beetle Onthophagus taurus by manipulating the quality of dung provided for larval growth and development. We show that the influence of larval nutrition differed considerably across three different trait classes (sexual, nonsexual and genital). The size of all nonsexual traits varied with dung quality but their allometric slopes remained unchanged. Relative horn length and allometry, but not absolute horn length, showed a high degree of plasticity with differences in dung quality. In contrast, both absolute size and allometry of genitalia were largely unresponsive to changes in dung quality. Male genitalia exhibited intermediate levels of phenotypic variation and lower allometric slopes than both horns and nonsexual traits. Thus, our findings provide little support for good genes hypotheses of genital evolution. We use our findings to discuss a developmental mechanism and selection pressures that may prevent the condition-dependent expression of genitalia.     

Male morph predicts investment in larval immune function in the dung beetle, Onthophagus taurus

Investment in immunity is costly, so that resource-based trade-offsbetween immunity and sexually selected ornaments might be expected.The amount of resources that an individual can invest in eachtrait will be limited by the total resources available to them.It would therefore be informative to investigate how investmentin immune function changes during growth or production of thesexual trait as resources are diverted to it. Using the dungbeetle, Onthophagus taurus, which displays both sexual and maledimorphism in horn size, we examined changes in one measureof immune function, phenoloxidase (PO) activity, in the hemolymphof larvae prior to and during horn growth. We found that POlevels differed between small- and large-horned males throughoutthe final instar prior to the point where investment in horngrowth was taking place. PO levels in females were intermediateto the 2 male morphs. These differences could not be accountedfor by differences in condition, measured as hemolymph proteinlevels and weight. We suggest that the observed differencesmight be associated with sex- and morph-specific variation injuvenile hormone levels.     

Between-partner concordance of vertically transmitted gut microbiota diminishes reproductive output in the dung beetle Onthophagus taurus

In this study, we explored the potential contribution of the gut microbiome to reproductive isolation in tunnelling dung beetles, using Onthophagus taurus (Schreber, 1759) and its sister species O. illyricus (Scopoli, 1763) as a model system (Coleoptera: Scarabaeidae: Scarabaeinae: Onthophagini). Gut microbiota play critical roles in normative development of these beetles, and are vertically inherited via a maternally derived faecal pellet called the pedestal. We first compared the developmental outcomes of individuals reared with pedestals derived from either the same or the sister species (Self and Cross inoculation treatments, respectively). We then crossed the resulting adult O. taurus in three combinations (Self female X Self male; Self female X Cross male; Cross female X Self male). We predicted that if the vertically transmitted gut microbiome plays a role in reproductive isolation by facilitating species recognition, the Self X Self line would have improved reproductive outcomes compared to the lines in which partners had mismatched gut microbiomes. Instead, we found that between-partner concordance of maternally transmitted gut microbiota resulted in fewer offspring, and that this reduction was due to partial pre-copulatory isolation as evidenced by reduced sperm transfer in the Self X Self line. This pattern is consistent either with microbiome-mediated familiarity/kin recognition, or with absence of mate choice in crosses with mismatched microbiomes. We discuss our results in the light of recent research on the influence of extracellular microbial symbionts over insects' mating preferences.     

Relative influence of male and female genital morphology on paternity in the dung beetle Onthophagus taurus

Studies of fertilization success have demonstrated that maleeffects are often a strong and important source of variationin P₂ (the proportion of offspring that are fertilized by thesecond male to mate). More recently there has been emphasison female processes that occur during and after copulation thatmight bias the outcome of male-male interactions. Here we usedthe sterile male technique to evaluate whether female genitalmorphology influences the repeatability of P₂ when the samepair of male dung beetles, Onthophagus taurus, copulated witha series of full-sib females or unrelated females that wereall unrelated to the male pair. Repeatability estimates of measuresof female genital morphology showed that full-sib females variedless in their genital morphology than did unrelated females.Therefore, if female genital traits are an important sourceof variation in male fertilization success, P₂ should be morerepeatable across full-sib than unrelated females. Contraryto this prediction, we show that the repeatability of P₂ didnot differ between female groups. Moreover, specific dimensionsof the female genitalia (sclerotized vagina and bursa) did notcontribute significantly to variance in P₂. In contrast, maleeffects had consistent and repeatable influences on paternityacross females. These were partly explained by variation inthe morphology of male genital sclerites.     

Proximate determination of male horn dimorphism in the beetle Onthophagus taurus (Coleoptera: Scarabaeidae)

The existence of discrete phenotypic variation within one sex poses interesting questions regarding how such intrasexual polymorphisms are produced and modified during the course of evolution. Approaching these kinds of questions requires insights into the genetic architecture underlying a polymorphism and an understanding of the proximate mechanisms determining phenotype expression. Here we explore the genetic underpinnings and proximate factors influencing the expression of beetle horns – a dramatic sexually selected trait exhibiting intramale dimorphism in many species. Two relatively discrete male morphs are present in natural populations of the dung beetle Onthophagus taurus (Scarabaeidae, Onthophagini). Males exceeding a critical body size develop a pair of long, curved horns on their heads, while those smaller than this critical body size remain essentially hornless. We present results from laboratory breeding experiments designed to assess the relative importance of inherited and environmental factors as determinants of male morphology. Using father–son regressions, our findings demonstrate that horn length and body size of male progeny are not predicted from paternal morphology. Instead, natural variation in an environmental factor, the amount of food available to larvae, determined both the body sizes exhibited by males as adults and the presence or absence of horns. The nonlinear scaling relationship between the body size and horn length of males bred in the laboratory did not differ from the pattern of variation present in natural populations, suggesting that nutritional conditions account for variation in male morphology in natural populations as well. We discuss our results by extending ideas proposed to explain the evolution of conditional expression of alternative phenotypes in physically heterogeneous environments toward incorporating facultative expression of secondary sexual traits. We use this synthesis to begin characterizing the potential origin and subsequent evolution of facultative horn expression in onthophagine beetles.     

The evolution of male genitalia: functional integration of genital sclerites in the dung beetle Onthophagus taurus

It is now widely recognized that sexual selection has been important in the rapid and divergent evolution of male genital morphology. However, distinguishing among putative mechanisms of sexual selection acting on male genital morphology represents a considerable challenge. Although there is growing evidence that variation in the size and/or shape of male genital structures can determine a male's success in gaining fertilizations, our knowledge of the functional morphology of male genitalia remains limited. Here we examine the functional morphology of genital sclerites that are known to influence paternity in the dung beetle Onthophagus taurus . We show that three of the sclerites form a functionally integrated unit that generates the tubular-shaped spermatophore and delivers its opening to the female's spermathecal duct. A fourth sclerite acts as a holdfast device during copulation. Our observations shed light on the mechanism by which these sclerites influence a male's paternity, and their patterns of phenotypic and genetic (co)variation.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 257–266.     

Intralocus tactical conflict: genetic correlations between fighters and sneakers of the dung beetle Onthophagus taurus

Males and females differ in their phenotypic optima for many traits, and as the majority of genes are expressed in both sexes, some alleles can be beneficial to one sex but harmful to the other (intralocus sexual conflict; ISC). ISC theory has recently been extended to intrasexual dimorphisms, where certain alleles may have opposite effects on the fitness of males of different morphs that employ alternative reproductive tactics (intralocus tactical conflict; ITC). Here, we use a half‐sib breeding design to investigate the genetic basis for ISC and ITC in the dung beetle Onthophagus taurus. We found positive heritabilities and intersexual genetic correlations for almost all traits investigated. Next, we calculated the intrasexual genetic correlation between males of different morphs for horn length, a sexually selected trait, and compared it to intrasexual correlations for naturally selected traits in both sexes. Intrasexual genetic correlations did not differ significantly between the sexes or between naturally and sexually selected traits, failing to support the hypothesis that horns present a reduction of intrasexual genetic correlations due to ITC. We discuss the implications for the idea of developmental reprogramming between male morphs and emphasize the importance of genetic correlations as constraints for the evolution of dimorphisms.     

Facultative paternal investment in the polyphenic beetle Onthophagus taurus: the role of male morphology and social context

Members of a population often differ significantly in theirparental investment. Such variation is generally believed tohave important consequences for mating system evolution andhas been suggested to play an important role in the evolutionof some secondary sexual traits and displays. Recent studiessuggest that individuals are able to adjust the intensity and kindof parental investment they provide according to the breedingconditions they encounter. As a consequence, between-individualvariation in parental investment may depend more on externalconditions than previously thought for these taxa. This mayhave important implications for current perspectives on therole of differential parental investment in the evolution andmaintenance of certain mating systems and sexual selection regimes.Here I quantify patterns of variation in paternal investmentas a function of social conditions in a species of beetle thatis dimorphic for male horn morphology. I demonstrate that undercertain conditions (namely, the absence of other males), paternalassistance covaries with male morphology, with horned males investingsubstantially more time in assisting females than hornless males.I also show that the magnitude of differences in paternal investmentbetween male morphs varies in response to external conditions.In the presence of other males, paternal assistance was negligiblefor both male morphs, who instead invested substantially andequally in mate-securing behaviors. I use my findings to discussthe significance of variation in paternal assistance for onthophaginemating systems and evaluate ideas proposed to explain the evolutionof alternative morphologies in the genus Onthophagus.     

Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae)

In nature, larvae of the dung beetle Onthophagus taurus (Schreber 1759) are confronted with significant variation in the availability of food without the option of locating new resources. Here we explore how variation in feeding conditions during the final larval instar affects larval growth and the timing of pupation. We found that larvae respond to food deprivation with a reduction in the length of the instar and premature pupation, leading to the early eclosion of a small adult. To achieve pupation, larvae required access to food for at least the first 5 days of the final instar (= 30% of mean third‐instar duration in control individuals), and had to exceed a weight of 0.08 g (= 58% of mean peak weight in control individuals). Larvae that were allowed to feed longer exhibited higher pupation success, but increased larval weight at the time of food deprivation did not result in increased pupation success except for larvae weighing > 0.14 g. Larvae responded to food deprivation by initiating and undergoing the same sequence of developmental events, requiring the same amount of time, as ad libitum‐fed larvae once those had reached their natural peak weight. Our results reveal a striking degree of flexibility in the dynamics and timing of larval development in O. taurus. They also suggest that premature exhaustion of a larva's food supply can serve as a cue for the initiation of metamorphosis. Premature metamorphosis in response to food deprivation has been documented in amphibians, but this is, to the best of our knowledge, the first time such a behaviour has been documented for a holometabolous insect. We discuss our findings in the context of the natural history and behavioural ecology of onthophagine beetles.     

Hormonal control of male horn length dimorphism in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae)

Male dung beetles (Onthophagus taurus) facultatively produce a pair of horns that extend from the base of the head: males growing larger than a threshold body size develop long horns, whereas males that do not achieve this size grow only rudimentary horns or no horns at all. Here we characterize the postembryonic development of these beetles, and begin to explore the hormonal regulation of horn growth. Using radioimmune assays to compare the ecdysteroid titers of horned males, hornless males, and females, we identify a small pulse of ecdysteroid which is present in both hornless males and females, but not in horned males. In addition, we identify a brief period near the end of the final (third) larval instar when topical applications of the juvenile hormone analog methoprene can switch the morphology of developing males. Small, normally hornless, males receiving methoprene during this sensitive period were induced to produce horns in 80% of the cases. We summarize this information in two models for the hormonal control of male dimorphism in horn length.     

Genital morphology and fertilization success in the dung beetle Onthophagus taurus: an example of sexually selected male genitalia

In animals with internal fertilization and promiscuous mating, male genitalia show rapid and divergent evolution. Three hypotheses have been suggested to explain the evolutionary processes responsible for genital evolution: the lock-and-key hypothesis, the pleiotropy hypothesis and the sexual-selection hypothesis. Here, we determine whether variation in male genital morphology influences fertilization success in the dung beetle Onthophagus taurus, as predicted by the sexual-selection hypothesis. Variation in four out of five genital sclerites of the endophallus influenced a male's fertilization success, supporting the general hypothesis that male genitalia can evolve under sexual selection. Furthermore, different genital sclerites were found to enhance first versus second male paternity, indicating that different sclerites serve offensive and defensive roles. Genital-trait variability was comparable to that in other species but was less variable than a non-genital sexually selected trait (head horns). We suggest that directional selection for genital elaboration may be countered by natural selection, which should favour genitalia of a size and shape necessary for efficient coupling and sperm transfer.     

Resource allocation during ontogeny is influenced by genetic,developmental and ecological factors in the horned beetle,Onthophagus taurus

Resource allocation trade-offs arise when developing organs are in competition for a limited pool of resources to sustain growth and differentiation. Such competition may constrain the maximal size to which structures can grow and may force a situation in which the evolutionary elaboration of one structure may only be possible at the expense of another. However, recent studies have called into question both the consistency and evolutionary importance of resource allocation trade-offs. This study focuses on a well-described trade-off between the horns and eyes of Onthophagus beetles and assesses the degree to which it is influenced by genetic, developmental and ecological conditions. Contrary to expectations, we observed that trade-off signatures (i) were mostly absent within natural populations, (ii) mostly failed to match naturally evolved divergences in horn investment among populations, (iii) were subject to differential changes in F₁ populations derived from divergent field populations and (iv) remained largely unaffected by developmental genetic manipulations of horn investment. Collectively, our results demonstrate that populations subject to different ecological conditions exhibit different patterns of, and differential plasticity in, resource allocation. Further, variation in ecological conditions, rather than canalized developmental mechanisms, may determine whether and to what degree morphological structures engage in resource allocation trade-offs.     

The evolution of male genitalia: patterns of genetic variation and covariation in the genital sclerites of the dung beetle Onthophagus taurus

Three main hypotheses, have been invoked to explain divergent genital evolution, the lock and key, pleiotropy, and sexual selection hypotheses, each of which make different predictions about how genital traits are inherited. Here we used a half-sib breeding design to examine the patterns of genetic variation and covariation between male genital sclerites, and their covariance with general body morphology in the dung beetle Onthophagus taurus. We found CV(A)'s and CV(P)'s were similar for both genital and general morphological traits and that CV(R)'s were large for both trait types. We found that male genital sclerites were negatively genetically correlated with general morphological traits. Variation in male genital morphology has direct implications for a male's fertilization success and the resulting sexual selection acting on male genitalia is predicted to maintain high levels of additive genetic variance. Contrary to this prediction, we found that individual genital sclerites all had low levels of additive genetic variance and large maternal and environmental sources of variation. Our data suggest that the genital sclerites in O. taurus are not inherited independently but as a genetically integrated unit. More importantly, the way the different sclerites function to influence male fertilization success reflects this genetic integration. Even though levels of V(A) in individual genital sclerites may be low, there may still be sufficient V(A) in multivariate trait space for selection to generate evolutionary change in the overall morphology of male genitalia.