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 .     

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.     

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.     

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.     

Male and female secondary sexual traits show different patterns of quantitative genetic and environmental variation in the horned beetle Onthophagus sagittarius

The expression of secondary sexual traits in females has often been attributed to a correlated response to selection on male traits. In rare cases, females have secondary sexual traits that are not homologous structures to secondary sexual traits in males and are thus less likely to have evolved in females because of correlated selection. In this study, we used the dung beetle Onthophagus sagittarius, a species with sex‐specific horns, to examine the environmental and quantitative genetic control of horn expression in males and females. Offspring subjected to different brood mass manipulations (dung addition/removal) were found to differ significantly in body size. Brood mass manipulation also had a significant effect on the length of male horns; however, female horn length was found to be relatively impervious to the treatment, showing stronger patterns of additive genetic variance than males. We found no correlations between horn expression in males and females. We therefore conclude that the horns of O. sagittarius females are unlikely to result from genetic correlations between males and females. Rather, our data suggest that they may be under independent genetic control.     

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.     

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.     

Brood ball size but not egg size correlates with maternal size in a dung beetle,Onthophagus atripennis

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Asymmetric competition in cattle dung between two species of Onthophagus dung beetle and the bush fly, Musca vetustissima

Abstract.

• 1 Competition in cattle dung pads between two dung beetles, Onthophagus ferox Harold and Onthophagus binodis Thunberg, and the bush fly, Musca vetustissima Walker, was investigated in laboratory experiments, to determine why spring fly abundance in the field did not fall following the introduction of O. binodis.
• 2 At low beetle densities, the number of eggs laid by each species was reduced by the second species. A similar amount of dung was buried by each species alone or by both together.
• 3 At high beetle densities O. binodis egg production was substantially affected by each additional O.ferox, but O.ferox egg production was not affected by each additional O.binodis. Asymmetric competition occurred because O.ferox buried more dung than O.binodis, and a greater proportion in day 1 (pre-emptive dung burial).
• 4 O.ferox caused greater M. vetustissima egg-puparia mortality than O. binodis. Mortality mostly occurred in young M. vetustissima larvae less than 1 day old. Total egg-puparia fly mortality was correlated better with the dung buried on day 1 than dung buried on day 8 (pre-emptive dung burial). O.binodis did not add to fly mortality by O.ferox at high densities because of asymmetric competition between the beetles.

     

No fecundity cost of female secondary sexual trait expression in the horned beetle Onthophagus sagittarius

Typically males bear the products of sexual selection in the form of ornaments and/or weapons used to compete for and attract females. Secondary sexual traits in females have been thought of as the product of correlated responses to sexual selection on males. However, there is increasing phylogenetic evidence that female secondary sexual traits can arise independently of selection on males, and may be subject to sexual selection. Theoretical models of the evolution of female ornamentation via male mate choice have assumed that females suffer a cost of ornament expression via reduced fecundity, and hence female ornaments are less likely to evolve than male ornaments. In the dung beetle Onthophagus sagittarius, there has been an independent evolutionary origin of horns in females that are qualitatively different from the horns produced by males. We use this system as a model to examine the costs of horn expression for females within a life-history context. We identified a longevity cost of reproduction for females that was independent of horn expression. Large females lived longer, and after controlling for lifespan, had a higher lifetime fecundity, and invested more heavily in maternal provisioning than did small females. We found no evidence of a cost to females of investment in horns. Rather, the rate of increase in fecundity and horn expression with body size were equal, so that absolute horn size provides an accurate indicator of body size and maternal quality. The effects we observe were independent of female contest competition and/or male mate choice, which were excluded in our experimental protocol. However, we speculate on the potential functional contributions female horns might make to female fitness.     

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.     

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.     

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.     

Sub-lethal effects of moxidectin on the Neotropical dung beetle Onthophagus landolti Harold (Coleoptera: Scarabaeinae)

Macrocyclic lactones can have adverse effects in dung beetles exposed to manure containing them. An assessment of the survival and fertility of adult Onthophagus landolti Harold fed with manure from cows treated with moxidectin was performed, as well as the emergence rate of the imagoes from the masses. Three cows (Bos indicus x B. taurus) were subcutaneously injected with 1% moxidectin (0.2 mg kg^?1 b.w.) and another three were injected with 10% moxidectin (1.0 mg/kg^?1 b.w.). Manure was collected from these animals one day prior to moxidectin administration, five days post-treatment in the 1% and 10% treatments, and fourteen days in the 10% treatment. Four bioassays were done: a control using manure without moxidectin; 1% moxidectin at five days post-treatment; 10% moxidectin at five days post-treatment; and 10% moxidectin at fourteen days post-treatment. In each replicate, for each pair of adult O. landolti was daily fed with 30 g manure according to the treatments. No lethal effects were observed in any of the four treatments. Sub-lethal effects (P < .05) were present in the 10% moxidectin treatments at five and fourteen days post-treatment. Fecundity was reduced by 78.2% at five days and 54.9% at fourteen days, and imago emergence was negatively affected at both times. Current moxidectin application methods may have negative effects on the environmental services provided by dung beetles, and therefore need to be modified to minimize any impacts they might have on these vital members of tropical livestock systems.     

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.     

Effect of dung burial by the dung beetle Bubas bison on numbers and viability of Cryptosporidium oocysts in cattle dung

Cryptosporidium oocysts were inoculated into fresh dung (∼1.2 × 10⁴ oocysts per gram wet weight) and fed to dung beetles to assess the effect of dung burial by the dung beetle Bubas bison on the distribution of the oocysts in small cores of soil in the laboratory. The experiment consisted of five replicates of each of two treatments; controls (dung but no dung beetles) and the experimental treatment (inoculated dung and seven pairs of dung beetles). After 5 days, when approximately 90% of the dung was buried, the surface and buried dung was recovered and subsampled. The oocysts in the subsamples were recovered and enumerated using qPCR. Oocyst viability was evaluated using an assay based on the exclusion or inclusion of two fluorogenic vital dyes, 4′,6-diamidino-2-phenylindole (DAPI) and propidium iodide (PI). Results revealed that overall 13.7% of oocysts remained on the surface and 86.3% of oocysts were buried. The viability of oocysts in buried dung was only 10% compared to oocysts the surface dung (58%). Therefore, widespread dung burial by B. bison during the winter months could substantially reduce the numbers of Cryptosporidium oocysts available to be washed into waterways following winter rains.     

Good genes and sexual selection in dung beetles (Onthophagus taurus): genetic variance in egg-to-adult and adult viability

Whether species exhibit significant heritable variation in fitness is central for sexual selection. According to good genes models there must be genetic variation in males leading to variation in offspring fitness if females are to obtain genetic benefits from exercising mate preferences, or by mating multiply. However, sexual selection based on genetic benefits is controversial, and there is limited unambiguous support for the notion that choosy or polyandrous females can increase the chances of producing offspring with high viability. Here we examine the levels of additive genetic variance in two fitness components in the dung beetle Onthophagus taurus. We found significant sire effects on egg-to-adult viability and on son, but not daughter, survival to sexual maturity, as well as moderate coefficients of additive variance in these traits. Moreover, we do not find evidence for sexual antagonism influencing genetic variation for fitness. Our results are consistent with good genes sexual selection, and suggest that both pre- and postcopulatory mate choice, and male competition could provide indirect benefits to females.     

Effects of maternal diet quality on offspring performance in the rove beetle Tachyporus hypnorum

Abstract.  1. The reproductive output of an individual is known to be influenced by diet quality, but the quality of the parent's diet can also influence the performance of the offspring. Dietary maternal effects may interact with the effects of the offspring's diet to produce a variety of response patterns.
2. Maternal effects were investigated in a polyphagous predator, the rove beetle Tachyporus hypnorum , using three single-species diets: two low-quality diets consisting of the aphids Sitobion avenae and Rhopalosiphum padi , and the high-quality control Drosophila melanogaster diet. Offspring of females fed these diets were raised on the same monotypic diets and allowed to reproduce. Several fitness parameters were measured to indicate possible maternal effects in both F1 and F2 generations.
3. Maternal diet effects in F1 were found in egg size, hatching success, time to hatching, larval development time, larval survival, and sex ratio. Both aphid diets resulted in smaller eggs. A diet of R. padi resulted in reduced hatching success, longer time spent in the egg stage, and a female-biased sex ratio. A maternal diet of R. padi also prolonged larval development on S. avenae diet, while a maternal diet of S. avenae decreased survival on the R. padi diet. These effects were independent of egg size.
4. A maternal diet of R. padi enhanced the survival of F1 larvae raised on the same diet. Developmental selection operating through a high egg mortality may be the explanation for this seemingly positive effect.
5.  Sitobion avenae alone caused a significant reduction in the hatching success of F2 eggs, thus revealing grandmaternal effects.
6. The prediction that polyphagous predators are less likely to evolve adaptive maternal effects is supported by the fact that none of the documented maternal effects could be interpreted as adaptive.