Search bioRxiv⌕ Search

Biology subjects

Oettler, J.

Publications and source records attributed to Oettler, J..

8 recordsLinked to original sources

Metabolic plasticity supports a flexible nutritional symbiosis in Cardiocondyla ants

Nutritional symbioses have repeatedly evolved in insects, yet how hosts regulate these partnerships to balance benefits across development and environments remains unclear. Ants provide an exceptional system to address this question, as several lineages maintain ancient symbionts that can be naturally lost without harming the host. Using Cardiocondyla obscurior, which carries and occasionally loses the vertically transmitted symbiont Cand. Westeberhardia cardiocondylae, we reveal the regulatory dynamics and function of this labile association. Symbionts provide shikimate-derived nutrients that enhance colony resilience under protein limitation, while hosts actively regulate symbiont abundance during protein scarcity and cuticle formation to optimise resource allocation. In the symbionts absence, ants compensate by upregulating genes enabling tyrosine acquisition from external sources. This metabolic flexibility allows colonies to exploit symbiont-derived and environmental nutrients, sustaining both growth and survival across nutritional contexts. Our findings reveal dynamic host regulation as a mechanism sustaining the persistence and adaptability of ancient symbioses.

ecology↗

Darwin's "neuters" and the evolution of the sex continuum in a superorganism

Ant castes are an amazing example of phenotypic plasticity. In worker-destined embryos of the ant Cardiocondyla obscurior, the default female developmental trajectory is interrupted even before the gonadal precursor cells acquire a sexual identity. miRNA and mRNA expression in embryos reveal three distinct phenotypic entities: males, females, and "neuters", as Darwin coined the worker caste in "On the Origin of Species". Based on these results we propose that haplodiploidy, in conjunction with insect sex determination, allows for the expression of a third dimension on the sex continuum, thus facilitating the evolution of individuals which develop traits their parents do not have. One sentence summarySex and caste differentiation begin during the same embryonic developmental window in the ant Cardiocondyla obscurior.

evolutionary biology↗

Sex- and caste-specific developmental responses to juvenile hormone in an ant with maternal caste determination

Queen-worker caste polyphenism in social insects is a prime example for developmental plasticity. Most of what we know about caste development comes from studies of the honeybee, in which female caste is determined during larval development and workers retain functional ovaries. The ant genus Cardiocondyla is one of only few genera in which complete worker sterility has evolved, so that adult workers completely lack reproductive organs. In C. obscurior, queen- and worker-destined individuals are distinct in their development by late-embryogenesis, and castes can be distinguished in a non-invasive manner from this stage onwards. This provides the opportunity to investigate the degree of flexibility in caste development in a species with early caste determination. Using topical juvenile hormone treatment, a method known to influence caste determination and differentiation in some species, we investigated whether hormone manipulation affects the development and growth of queen and worker-destined late-stage embryos and larvae, as well as of early-stage embryos which cannot yet be distinguished by caste. We found no effect of hormone treatment on female caste ratios or body sizes in any of the treated stages, even though individuals reacted to heightened hormone availability with increases in the expression of kruppel-homolog 1, a conserved JH first-response gene. In contrast, hormone treatment resulted in the emergence of significantly larger males. These results show that in C. obscurior, early, presumably maternal caste determination leads to irreversible and highly-canalized caste-specific development and growth.

zoology↗

The indispensable soma of Cardiocondyla obscurior ants

The evolutionary mechanisms that shape aging in social insects are not well understood. It is commonly assumed that queens live long and prosperous, while workers are regarded as a short-lived disposable caste because of their low reproductive potential. Queens of the ant Cardiocondyla obscurior gain high fitness late in life by increasing investment into sexual offspring as they age. This results in strong selection against senescence until shortly before death. Here, we show that workers have the same lifespan and shape of aging as queens, even though workers lack reproductive organs and cannot gain direct fitness. Under consideration of the prevailing aging theories and the biology of the species, we hypothesize that programmed aging has possibly evolved under kin selection. Impact statementMorphologically distinct fertile queen and sterile worker castes in the model ant Cardiocondyla obscurior show the same pace and shape of aging, contradicting the paradigm of queen/worker lifespan divergence in social insects.

evolutionary biology↗

Crystalline deposits reveal caste identity of late embryos and larvae of the ant Cardiocondyla obscurior

Ant queens and workers commonly engage in conflict over reproductive allocation because they have different fitness optima. How such conflicts are resolved depends on the power that each party of interest holds. Here, we show that queens have control over caste allocation in the ant Cardiocondyla obscurior. With the discovery of crystalline deposits that allow the identification of queens and workers across the entire course of development, we demonstrate that caste fate is irreversibly determined in the egg stage. Comparison of queen and worker-destined eggs and larvae revealed size and weight differences in late development, but no discernible differences in traits that may be used in social interactions, including hair morphology and cuticular odors. In line with this lack of caste-specific traits, adult workers treated developing queens and workers indiscriminately, even in the presence of a fertile queen. Together with previous studies showing queen control over sex allocation, these results provide evidence that conflict over reproductive allocation is absent in this ant.

evolutionary biology↗

Social aging: Late-life fitness gains explain the absence of a selection shadow in ants

A key hypothesis for the occurrence of senescence is a decrease in the selection strength because of low late-life fitness - the so-called selection shadow. However, in social insects, aging is considered a plastic trait and senescence seems to be absent. By life-long tracking of 102 ant colonies, we find that queens increase the production of sexuals in late life regardless of their absolute lifespan or worker investment. This indicates a genetically accommodated adaptive shift towards increasingly queen-biased caste ratios over the course of a queens life. Furthermore, mortality decreased with age, supporting the hypothesis that aging is adaptive. We argue that selection for late life reproduction diminishes the selection shadow of old age and leads to the apparent absence of senescence in ants, in contrast to most iteroparous species. Significance StatementSocial insects are extraordinary with regard to the absolute age of queens of some species as well as the age differences between queens and short-lived workers. Yet, ultimate causes explaining these aging patterns remain poorly understood. By manipulating the investment ratio into queens and workers we studied the effect on lifespan and temporal reproductive investment of queens. We show that queens shift to the production of sexuals late in life, independent of social context (colony size) or individual quality (reproductive output and lifespan). Such late fitness gains result in maintenance in the selection strength with age, and thus explains the absence of senescence in queens.

evolutionary biology↗

Gene co-expression network reveals highly conserved, well-regulated anti-ageing mechanisms in old ant queens.

Evolutionary theories of ageing predict a reduction in selection efficiency with age, a so-called selection shadow, due to extrinsic mortality decreasing effective population size with age. Classic symptoms of ageing include a deterioration in transcriptional regulation and protein homeostasis. Understanding how ant queens defy the trade-off between fecundity and lifespan remains a major challenge for the evolutionary theory of ageing. It has often been discussed that the low extrinsic mortality of ant queens, that are generally well protected within the nest by workers and soldiers, should reduce the selection shadow acting on old queens. We tested this by comparing strength of selection acting on genes upregulated in young and old queens of the ant, Cardiocondyla obscurior. In support of a reduced selection shadow, we find old-biased genes to be under strong purifying selection. We also analysed a gene co-expression network (GCN) with the aim to detect signs of ageing in the form of deteriorating regulation and proteostasis. We find no evidence for ageing. In fact, we detect higher connectivity in old queens indicating increased transcriptional regulation with age. Within the GCN, we discover five highly correlated modules that are upregulated with age. These old-biased modules regulate several anti-ageing mechanisms such as maintenance of proteostasis, transcriptional regulation and stress response. We observe stronger purifying selection on central hub genes of these old-biased modules compared to young-biased modules. These results indicate a lack of transcriptional ageing in old C. obscurior queens possibly facilitated by strong selection at old age and well-regulated anti-ageing mechanisms. Significance StatementUnderstanding the exceptional longevity of ant queens and how they defy the trade-off between fecundity and lifespan remains a major challenge for the evolutionary theory and molecular biology of ageing. In this study we offer several clues as to how this occurs on a molecular level in C. obscurior queens. Specifically, we believe a reduction in the selection shadow due to low extrinsic mortality, has allowed the evolution of well-regulated anti-ageing mechanisms. Consequently, we suggest several promising starting points for future research into the poorly understood phenomenon of extreme longevity in ant queens. Making progress in this field will not only allow us to better understand longevity and fertility in social insects but may also offer interesting research strategies for human ageing.

evolutionary biology↗

Cytoplasmic incompatibility between Old and New World populations of a tramp ant

As we enter the Anthropocene, the evolutionary dynamics of species will change drastically, and as yet unpredictably, due to human activity. Already today, increases in global human traffic have resulted in the rapid spread of species to new areas, leading to the formation of geographically isolated populations. These go on to evolve in allopatry, which can lead to reproductive isolation, and potentially, the formation of new species. Surprisingly, little is known about such eco-evolutionary processes in ants, even though numerous invasive ant species are globally distributed in geographically isolated populations. Here, we describe the first case of cytoplasmic incompatibility (CI) between populations of a cosmotropic distributed tramp ant with Asian roots, Cardiocondyla obscurior, which has acquired a novel Wolbachia strain in the New World. Our study uncovers the first symbiont-induced mechanism of reproductive isolation in ants, providing a novel perspective on the biology of globally distributed ants.

evolutionary biology↗