Sandra Steiger

The origin and dynamic evolution of chemical information transfer

Although chemical communication is the most widespread form of communication, its evolution and diversity are not well understood. By integrating studies of a wide range of terrestrial plants and animals, we show that many chemicals are emitted, which can unintentionally provide information (cues) and, therefore, act as direct precursors for the evolution of intentional communication (signals). Depending on the content, design and the original function of the cue, there are predictable ways that selection can enhance the communicative function of chemicals. We review recent progress on how efficacy-based selection by receivers leads to distinct evolutionary trajectories of chemical communication. Because the original function of a cue may channel but also constrain the evolution of functional communication, we show that a broad perspective on multiple selective pressures acting upon chemicals provides important insights into the origin and dynamic evolution of chemical information transfer. Finally, we argue that integrating chemical ecology into communication theory may significantly enhance our understanding of the evolution, the design and the content of signals in general.

The Coolidge effect, individual recognition and selection for distinctive cuticular signatures in a burying beetle

The ability to recognize individuals is an important aspect of social interactions, but it can also be useful to avoid repeated matings with the same individual. The Coolidge effect is the progressive decline in a males propensity to mate with the same female combined with a heightened sexual interest in new females. Although males that recognize previous partners and show a preference for novel females should have a selective advantage as they can distribute sperm evenly among the females they encounter, there are few invertebrate examples of the Coolidge effect. Here we present evidence for this effect in the burying beetle Nicrophorus vespilloides and examine the mechanism underlying the discrimination between familiar and novel mates. Burying beetles feed and reproduce on vertebrate carcasses, where they regularly encounter conspecifics. Males showed greater sexual interest in novel females (virgin or mated) than in females they had inseminated before. The application of identical cuticular extracts allowed us to experimentally create females with similar odours, and male responses to such females demonstrated that they use female cuticular patterns for discrimination. The chemical analysis of the cuticular profile revealed greater inter-individual variation in female than in male cuticular patterns, which might be due to greater selection on females to signal their individual identity.

Bigger mothers are better mothers: disentangling size-related prenatal and postnatal maternal effects

Despite a vast literature on the factors controlling adult size, few studies have investigated how maternal size affects offspring size independent of direct genetic effects, thereby separating prenatal from postnatal influences. I used a novel experimental design that combined a cross-fostering approach with phenotypic manipulation of maternal body size that allowed me to disentangle prenatal and postnatal maternal effects. Using the burying beetle Nicrophorus vespilloides as model organism, I found that a mothers body size affected egg size as well as the quality of postnatal maternal care, with larger mothers producing larger eggs and raising larger offspring than smaller females. However, with respect to the relative importance of prenatal and postnatal maternal effects on offspring growth, only the postnatal effects were important in determining offspring body size. Thus, prenatal effects can be offset by the quality of postnatal maternal care. This finding has implications for the coevolution of prenatal and postnatal maternal effects as they arise as a consequence of maternal body size. In general, my study provides evidence that there can be transgenerational phenotypic plasticity, with maternal size determining offspring size leading to a resemblance between mothers and their offspring above and beyond any direct genetic effects.

Unearthing carrion beetles' microbiome: characterization of bacterial and fungal hindgut communities across the Silphidae

Carrion beetles (Coleoptera, Silphidae) are well known for their behaviour of exploiting vertebrate carcasses for nutrition. While species in the subfamily Silphinae feed on large carcasses and on larvae of competing scavengers, the Nicrophorinae are unique in monopolizing, burying and defending small carrion, and providing extensive biparental care. As a first step towards investigating whether microbial symbionts may aid in carcass utilization or defence, we characterized the microbial hindgut communities of six Nicrophorinae (Nicrophorus spp.) and two Silphinae species (Oiceoptoma noveboracense and Necrophila americana) by deep ribosomal RNA amplicon sequencing. Across all species, bacteria in the family Xanthomonadaceae, related to Ignatzschineriao larvae, were consistently common, and several other taxa were present in lower abundance (Enterobacteriales, Burkholderiales, Bacilli, Clostridiales and Bacteroidales). Additionally, the Nicrophorinae showed high numbers of unusual Clostridiales, while the Silphinae were characterized by Flavobacteriales and Rhizobiales (Bartonella sp.). In addition to the complex community of bacterial symbionts, each species of carrion beetle harboured a diversity of ascomycetous yeasts closely related to Yarrowia lipolytica. Despite the high degree of consistency in microbial communities across the Silphidae—specifically within the Nicrophorinae—both the fungal symbiont phylogeny and distance‐based bacterial community clustering showed higher congruence with sampling locality than host phylogeny. Thus, despite the possibility for vertical transmission via anal secretions, the distinct hindgut microbiota of the Silphidae appears to be shaped by frequent horizontal exchange or environmental uptake of symbionts. The microbial community profiles, together with information on host ecology and the metabolic potential of related microorganisms, allow us to propose hypotheses on putative roles of the symbionts in carcass degradation, detoxification and defence.

Cuticular hydrocarbons as a basis for chemosensory self-referencing in crickets: a potentially universal mechanism facilitating polyandry in insects.

Females of many species obtain benefits by mating polyandrously, and often prefer novel males over previous mates. However, how do females recognise previous mates, particularly in the face of cognitive constraints? Female crickets appear to have evolved a simple but effective solution: females imbue males with their own cuticular hydrocarbons (CHCs) at mating and utilise chemosensory self-referencing to recognise recent mates. Female CHC profiles exhibited significant additive genetic variation, demonstrating that genetically unique chemical cues are available to support chemosensory self-referencing. CHC profiles of males became more similar to those of females after mating, indicating physical transfer of CHCs between individuals during copulation. Experimental perfuming of males with female CHCs resulted in a female aversion to males bearing chemical cues similar to their own. Chemosensory self-referencing, therefore, could be a widespread mechanism by which females increase the diversity of their mating partners.

Correlated changes in breeding status and polyunsaturated cuticular hydrocarbons: the chemical basis of nestmate recognition in the burying beetle Nicrophorus vespilloides?

Nestmate recognition in eusocial insects has received a lot of attention in the last decades. Recognition in subsocial species, in contrast, has been ignored almost completely and consequently, and little is known about proximate mechanisms of recognition in subsocial systems. We studied one subsocial species, the biparental brood caring burying beetle Nicrophorus vespilloides, an interesting model organism for studies of recognition because of its ability to discriminate between breeding partners and conspecific competitors. Recognition appears to be based on a chemical cue closely linked to the breeding status of individuals. Breeding and non-breeding beetles consistently differ in their relative proportions of polyunsaturated cuticular hydrocarbons. To investigate the function of these polyenes in the burying beetles’ recognition system, we quantified their concentration on the cuticle during the early state of a breeding attempt and tested the response of breeding beetles in corresponding behavioural experiments. We observed a rapid increase in the proportion of polyunsaturated hydrocarbons of both males and females after they were provided with a carcass suitable for reproduction. Furthermore, we found that the relative amount of polyenes on an individual’s surface was closely correlated with its chance of being accepted as breeding partner. Our results support the idea that polyunsaturated hydrocarbons are involved in breeding partner recognition in N. vespilloides, functioning as a signal that conveys information about the individual’s breeding status. Breeding females have greater amount of polyenes than breeding males, and females ingest more carrion during the first days on the carcass, which supports our hypothesis that precursors for the respective polyenes are derived from ingested carrion.

Sex, offspring and carcass determine antimicrobial peptide expression in the burying beetle.

The burying beetle Nicrophorus vespilloides has emerged as a model system for the investigation of adaptations that allow the utilization of carrion as a diet and as a resource for reproduction. The survival of beetles and their offspring given their exposure to soil-dwelling and cadaver-borne microbes requires mechanisms that reduce bacterial contamination in the diet and that achieve sanitation of the microhabitat. To explore the role of antimicrobial peptides (AMPs) in this context, we analyzed burying beetle males and females at different stages of their breeding cycle using the RNA-Seq and proteomics approaches. To address variation in immune functions, we investigated the impact of adult sex, the presence or absence of offspring (social context), and the presence of carrion (environmental context) on the expression of the identified immune effector genes. We found that particular AMPs are sex-specific and tightly regulated by the presence of a carcass or offspring and identified the two most context-dependent antimicrobial proteins in anal secretions. The context-specific expression dynamics of particular AMPs and lysozymes reveals a complex regulatory system, reflecting adaptations to specific ecological niches. This study highlights how burying beetles cope with microorganisms found on carrion and identifies candidates for both internal and external immunity.

The Role of Sexual Selection in the Evolution of Chemical Signals in Insects

Chemical communication is the most ancient and widespread form of communication. Yet we are only beginning to grasp the complexity of chemical signals and the role they play in sexual selection. Focusing on insects, we review here the recent progress in the field of olfactory-based sexual selection. We will show that there is mounting empirical evidence that sexual selection affects the evolution of chemical traits, but form and strength of selection differ between species. Studies indicate that some chemical signals are expressed in relation to an individual’s condition and depend, for example, on age, immunocompetence, fertility, body size or degree of inbreeding. Males or females might benefit by choosing based on those traits, gaining resources or “good genes”. Other chemical traits appear to reliably reflect an individual’s underlying genotype and are suitable to choose a mating partner that matches best the own genotype.

(E)-Methylgeranate, a chemical signal of juvenile hormone titre and its role in the partner recognition system of burying beetles

In recent years, studies have shown that animals can communicate their physiological state or condition by means of chemical signals. However, as the chemicals involved in the condition-dependent signals have rarely been identified, evolutionary mechanisms that ensure their reliability are not well understood. We identified a volatile chemical signal that may serve as a reliable indicator of hormonal state in burying beetles, and is involved in their partner recognition system. Burying beetles reproducing on carcasses are able to distinguish between their breeding partners and infanticidal conspecifics. This discrimination depends on breeding status, which is positively linked to juvenile hormone III (JH III) titre. Breeding Nicrophorus vespilloides beetles, in contrast to nonbreeding ones, emitted considerable amounts of (E)-methylgeranate. The amount of emitted (E)-methylgeranate was positively correlated with juvenile hormone titres known from other burying beetle studies. Moreover, our behavioural experiments showed that dummies treated with methylgeranate induced tolerant behaviour, whereas control dummies were treated aggressively. The fact that (E)-methylgeranate and JH III share a conspicuous structural similarity and the same biosynthetic pathway may explain how the reliability of the signal for JH titre is ensured. We discuss the implications of our results in the light of theoretical work on the evolution of chemical communication, particularly on the origin of chemical signals.

A hormone-related female anti-aphrodisiac signals temporary infertility and causes sexual abstinence to synchronize parental care

The high energetic demand of parental care requires parents to direct their resources towards the support of existing offspring rather than investing into the production of additional young. However, how such a resource flow is channelled appropriately is poorly understood. In this study, we provide the first comprehensive analysis of the physiological mechanisms coordinating parental and mating effort in an insect exhibiting biparental care. We show a hormone-mediated infertility in female burying beetles during the time the current offspring is needy and report that this temporary infertility is communicated via a pheromone to the male partner, where it inhibits copulation. A shared pathway of hormone and pheromone system ensures the reliability of the anti-aphrodisiac. Female infertility and male sexual abstinence provide for the concerted investment of parental resources into the existing developing young. Our study thus contributes to our deeper understanding of the mechanisms underlying adaptive parental decisions.