Light up the fly: Drosophila as a non-social model in insect sociobiology

Eusocial breeding systems are characterized by a reproductive division of labour. For many social taxa, the queen signals her fecundity to her daughters via a pheromone, which renders them sterile. Solitary insects, in contrast, lack social organization and their personal reproduction is not regulated by social cues. Despite these radically different breeding habits between these two taxa, one prediction from sociogenomic theory is that eusocial taxa evolved their complex caste system through co-option of pathways already present in solitary ancestors. In this thesis, I present a series of comparative experiments that provide support for these conserved genes and gene pathways that regulate reproduction in social versus non-social taxa. First, I show that distinctly non-social Drosophila melanogaster can respond to a highly social Apis mellifera pheromone (QMP) in a manner similar to sterile worker bees – namely, by turning off their ovaries and foregoing reproduction. Second, I show that this conspicuous interspecific response is conserved at a genetic level, where the presence of certain foraging alleles can elicit variable responses to the pheromone in a manner similar to that in the bee. Third, I suggest that solitary and eusocial species use a conserved olfactory signaling mechanism to elicit reproductive responses to QMP. Using mutant Drosophila lines and an RNAi-mediated screen of olfactory receptors, I identify five top receptors as candidates for the perception of QMP and subsequent reduced ovary phenotypes. Lastly, I use Drosophila to investigate the functional association between two opposing social cues, royal jelly and QMP and their ability to modulate ovarian development. These results showcase the power of the comparative approach in identifying genes and gene pathways involved in the regulation of worker sterility, and suggest that the genetic basis of characteristically eusocial behaviours like reproductive altruism, are conserved in non-social insects

Ant colonies: building complex organizations with minuscule brains and no leaders

Thus far the articles in the series JOD calls the “Organization Zoo” have employed the notion of a “zoo” metaphorically to describe an array of human institutions. Here we take the term literally to consider the design of the most complex organizations in the living world beside those of humans, a favorite of insect zoos around the world: ant colonies. We consider individuality and group identity in the functioning of ant organizations; advantages of a flat organization without hierarchies or leaders; self-organization; direct and indirect communication; job specialization; labor coordination; and the role of errors in innovation. The likely value and limitations of comparing ant and human organizations are briefly examined

Homo faber juvenalis: A Multidisciplinary Survey of Children as Tool Makers/Users

The overall goal of this paper is to derive a set of generalizations that might characterize children as tool makers/users in the earliest human societies. These generalizations will be sought from the collective wisdom of four distinct bodies of scholarship: lithic archaeology; juvenile chimps as novice tool users; recent laboratory work in human infant and child cognition, focused on objects becoming tools and; the ethnographic study of children learning their community’s tool-kit. The presumption is that this collective wisdom will yield greater insight into children’s development as tool producers and users than has been available to scholars operating within narrower disciplinary limits

The importance of direct fitness for helpers in advanced social societies

Social insect societies are characterized by a caste determined reproductive and non-reproductive division of labor. Usually, queens stay in the safe surrounding of the nest and produce offspring, while workers refrain from reproduction and care for the brood, forage or defend the nest. However, workers of many social insect species are principally capable of laying unfertilized eggs, which can develop into males. In cooperatively breeding birds or mammals, helpers forgo early reproduction to benefit from brood care experience or nest inheritance and thus, gain an increased direct fitness later in life. However, workers in highly social insect species as in many ants, bees and wasps, generally cannot inherit the nest and replace a fully fertile queen due to physiological restrictions, and the importance of direct fitness benefits for workers has long been neglected. Referring to Hamilton (1964b), it is assumed that ant workers refrain from direct fitness (their own produced offspring) to benefit from indirect fitness the offspring produced by the queen due to their help) and thereby, increase their inclusive fitness. Questions arose whether this is sufficient to explain a lifetime resignation from reproduction in social insect workers. Indeed, several studies report selfish behaviors like worker policing, egg dumping or the refusal of costly tasks, possibly to increase the chance for future direct fitness in individual workers. Here, we studied the importance of direct fitness for workers in the monogynous, monandrous ant Temnothorax crassispinus. We examined the reproductive success of workers by ovary dissections and genotyping workers and males from natural queenless and queenright colonies (chapter 2), and monitored the survival and productivity of queenless and queenright colonies for four years in captivity (chapter 3). We compared fitness traits of queen- and worker-produced males under near-natural and standardized conditions (chapter 4) and investigated whether males produced by workers in the absence of a queen, are accepted in queenright colonies during colony reunification before hibernation (chapter 5). Moreover, we hypothesized that the reproductive potential of young workers might induce selfishness and limit behavioral flexibility under pathogen threat (chapter 6) and examined the effect of selfish reproduction on sanitary behavior of the workers (chapter 7). Our studies show, that queen presence or absence, respectively did not affect ovary development in workers and that around 30% of the genotyped males were not produced by the estimated queen in natural colonies. Most males that were not produced by the queen, were produced by workers not related to the colony. Accordingly, the reproductive success of workers related to the queen seemed to be comparably low in nature but increased under laboratory conditions. Workers seem to be capable of increasing their direct fitness by the expulsion or killing of the queen and a reinforced reproduction afterwards. Queenless colonies were highly productive and persistent and sperm traits of worker-produced males varied only little from that of queen-produced males. Furthermore, larvae produced in queenless colony fragments could be readily integrated in queenright laboratory colonies during colony reunification before hibernation, and contributed considerably to male production in queenright colonies. However, the prospect of future reproductive success did not affect altruistic self-removal in health compromised workers, but microbiota growth seemed to be encouraged in queenless colonies when sanitary behavior is neglected

NEW INSIGHTS INTO THE FUNCTION AND DEVELOPMENT OF THE SOLDIER CASTE IN TERMITES

The evolution of nonreproductive castes is a defining characteristic of eusociality. The function and developmental regulation of the altruistic worker and soldier caste is the central element contributing to major advantages of eusociality over solitary animals. The soldier caste is the first evolved sterile caste in termites. Their primary function is believed to be colony defense. However, the function and development of termite soldiers remains largely unknown. Because of their apparent morphological adaptation for fighting and their limited behavior repertoire, our understanding of colony defense by termite soldiers is limited to their physical defense. In addition, we know little about the molecular mechanisms mediating soldier development. In Chapters 2 and 3 I discuss the role of the soldier caste under competition risk. By exposing the Eastern subterranean termite Reticulitermes flavipes to cues of a competitor termite species, I found that exposure to competitor cues reduced feeding, compromised growth and survival of R. flavipes workers. The presence of R. flavipes soldiers largely ameliorated these negative impacts. At the transcriptional level, R. flavipes soldiers can counteract the effects of competitor cues on worker head gene expression. This counteracting effect seems to be associated with genes in metabolism and immunity. These studies demonstrate that competition can affect a termite colony’s fitness by either competitors physically invading the colony and causing damage or cues from competitors inducing a stress response in termite colony members. More importantly, soldiers can contribute to colony fitness by physically engaging in combat, but also by enhancing colony members’ survival under competitor-cue exposure. In Chapter 4, I describe the molecular mechanism mediating soldier-caste differentiation. I cloned the full length cDNA sequence of the R. flavipes Methoprene-tolerance (Met) gene, a gene encoding a putative receptor for juvenile hormones. Using RNA interference, I studied the function of Met and found that this gene essentially mediates the JH-dependent soldier-caste differentiation in termites

The use of multilayer network analysis in animal behaviour

Network analysis has driven key developments in research on animal behaviour by providing quantitative methods to study the social structures of animal groups and populations. A recent formalism, known as \emph{multilayer network analysis}, has advanced the study of multifaceted networked systems in many disciplines. It offers novel ways to study and quantify animal behaviour as connected 'layers' of interactions. In this article, we review common questions in animal behaviour that can be studied using a multilayer approach, and we link these questions to specific analyses. We outline the types of behavioural data and questions that may be suitable to study using multilayer network analysis. We detail several multilayer methods, which can provide new insights into questions about animal sociality at individual, group, population, and evolutionary levels of organisation. We give examples for how to implement multilayer methods to demonstrate how taking a multilayer approach can alter inferences about social structure and the positions of individuals within such a structure. Finally, we discuss caveats to undertaking multilayer network analysis in the study of animal social networks, and we call attention to methodological challenges for the application of these approaches. Our aim is to instigate the study of new questions about animal sociality using the new toolbox of multilayer network analysis.Comment: Thoroughly revised; title changed slightl

Habitat Ecology and Primate Gregariousness in Nigeria's Gashaka Gumti National Park

Research presented in this thesis focusses on the interplay between plant and mammal communities within a unique West African biome: the mosaic savannah-forest habitat of the Gashaka-Kwano region in northeastern Nigeria. The major strands of investigation encompass habitat ecology and animal sociality as shaped by a significantly seasonal climate and revealed through analyses of a longitudinal data set. The research is part of the Gashaka Primate Project (www.ucl.ac.uk/gashaka), one of West Africa's largest conservation and research initiatives, founded in the year 2000. The project operates in Gashaka Gumti National Park (GGNP) – a last remaining wilderness in the ecoregion that still harbours a biodiverse flora and fauna. At GGNP, a pronounced fluctuation between an annual wet and dry season strongly influences the vegetation and corresponding wildlife as well as human subsistence. This marked climatic seasonality affects plant cover and fruit productivity, giving rise to a seasonal pattern of food availability that constrains wildlife ecology and shapes activity budgets and reproductive features. These dynamics are specifically explored with respect to an unhabituated community of chimpanzees, and two study troops of baboons – an entirely wild-feeding group, and another group that supplements its diet through crop-raiding. With respect to the latter, the thesis explores if and how constraints imposed by habitat seasonality can be buffered by the consumption of crops. The current investigation capitalizes on the project's longitudinal repositories of base-line data covering a 13–year period (2002–2014), which were compiled, cleaned and analysed. The resulting thesis is broken down into seven chapters: – Ch. 01 Research rationale. Importance of long-term data and focus on seasonality – Ch. 02 The Gashaka Primate Project. Long-term research in Gashaka Gumti National Park – Ch. 03 Seasonality in a savannah-forest mosaic. Climate and plant phenology – Ch. 04 Chimpanzee gregariousness. Influence of abundance and dispersion of food patches – Ch. 05 Baboon behaviour. Activity budgets and home range use – Ch. 06 Baboon demography and reproduction. Comparing wild-feeding and crop-raiding troops – Ch. 07 Outlook. Enabling research and conservation at a biodiversity hotspo