Asexual queen succession mediates an accelerated colony life cycle in the termite Silvestritermes minutus

Mixed modes of reproduction, combining sexual processes with thelytokous parthenogenesis, occur in all major clades of social insects. In several species of termites, queens maximize their genetic input into nondispersing replacement queens through parthenogenesis, while maintaining genetically diverse sterile offspring and dispersing reproductives via sexual reproduction. This so‐called asexual queen succession (AQS) has multiple independent origins and its presumed advantages are diverse as well, ranging from multiplication of colony reproductive potential to extension of its lifespan beyond that of the foundress. However, how AQS shapes colony life cycles under natural conditions remains poorly known. The neotropical termite Silvestritermes minutus inhabits small but conspicuous nests, offering a unique opportunity to investigate the impact of AQS on life history. We report on its breeding system, life cycle and sex allocation using social structure census in 137 nests and genotyping of 12 colonies at 12 microsatellite loci. We show that colonies are established by an outbred pair of primary reproductives. In less than 2 years, the foundress is replaced by multiple neotenic queens, arising mostly through automixis with central fusion. Sterile castes, male and most (93%) female dispersers are produced sexually. Colony reproduction is usually restricted to a single dispersal of alates with unbiased sex ratio, taking place after 3 years. We conclude that S. minutus benefits from AQS to maximize colony growth rate and alate production within a very short life cycle rather than to extend colony lifespan. This highlights the versatile role of AQS in different cases of its polyphyletic origin.     

Programmed aging of mammals: Proof of concept and prospects of biochemical approaches for anti-aging therapy

(i) In 2015-2017 we compared possible reasons for longevity of two mammalian highly social species, i.e. naked mole rats and humans. We proposed that in both cases longevity is a result of neoteny, prolongation of youth by deceleration of late ontogeny (Skulachev, V. P. (2015) Abst. 11th Conf. on Mitochondrial Physiology (MiP2015), Lucni Bouda, Czech Republic, pp. 64-66; Skulachev, V. P., Holtze, S., Vyssokikh, M. Y., Bakeeva, L. E., Skulachev, M. V., Markov, A. V., Hildebrandt, T. B., and Sadovnichii, V. A. (2017) Physiol. Rev., 97, 699-720). Both naked mole rats and humans strongly decreased the pressure of natural selection, although in two different manners. Naked mole rats preferred an “aristocratic” pathway when reproduction (and, hence, involvement in evolution) is monopolized by the queen and her several husbands. Huge number of subordinates who have no right to take part in reproduction and hence in evolution serves the small queen’s family. Humans used an alternative, “democratic” pathway, namely technical progress facilitating adaptation to the changing environmental conditions. This pathway is open to all humankind. (ii) As a result, aging as a mechanism increasing evolvability by means of facilitation of natural selection became unnecessary for naked mole rats and humans due to strong attenuation of this selection. This is apparently why aging became a counterproductive atavism for these two species and was strongly shifted to late ages. This shift is direct evidence of the hypothesis that aging is programmed, being the last step of late ontogeny. (iii) Further deceleration of aging for humans by means of neoteny is unrealistic since the development of neoteny probably takes million years. (iv) However, if biological aging is a program, an alternative and much simpler way to avoid it seems possible. We mean inhibition of an essential step of this program. (v) At present, the most probable scheme of the aging program assumes that it is a mechanism of slow poisoning of an organism by reactive oxygen species produced by mitochondria. If this is the case, a mitochondria-targeted antioxidant might be an inhibitor of the aging program. During the last 12 years, such an antioxidant, namely SkQ1, was synthesized and studied in detail in our group. It consists of plastoquinone and decyltriphenylphosphonium (a penetrating cation responsible for electrophoretic accumulation of SkQ1 in mitochondria). It was shown that long-term treatment with SkQ1 increased the lifespan of plants, fungi, invertebrates, fish, and mammals. Moreover, SkQ1 is effective in the therapy of various age-related diseases. It was also shown that a single SkQ1 injection could save life in certain models of sudden death of animals. (vi) A tentative scheme is proposed considering aging as a process of chronic phenoptosis, which eventually results in initiation of acute phenoptosis and death. This scheme also suggests that under certain conditions chronic phenoptosis can be neutralized by an anti-aging program that is activated by food restriction regarded by an organism as a signal of starvation. As for acute phenoptosis, it is apparently controlled by receptors responsible for measuring key parameters of homeostasis. The first experimental indications have been already obtained indicating that both chronic and acute phenoptosis are suppressed by SkQ1.     

Mechanisms of reproductive aging in the females

Aging is a developmental process occurring in all living organisms after reaching a critical developmental stage, characterized by progressive loss of functions until death. Different cells/tissues age differently depending on epigenetics and cell-cell interactions. While males maintain fertility for the most part of their life females only maintain reproductive ability for a short time compared with their lifespan. The interesting question is why and how the females lose fertility so quickly. There have been many hypotheses proposed from different perspectives and recent research has revealed unusual interactions between germ cells and somatic cells which may determine the lifespan of reproduction in the females. This review briefly discusses recent progress in reproductive aging in the well studied model, C. elegans, and focuses on the molecular mechanisms which may be conserved across all animals including humans.     

Colony size explains the lifespan differences between queens and workers in eusocial Hymenoptera

Eusocial Hymenoptera show a unique divergence in lifespan of queens and workers; queens belong to the longest lived insects while workers in most eusocial species have significantly shorter lives. The different phenotypes within a colony emerge through reproductive division of labour, which is a characteristic trait of eusocial animals. Division of labour as a measure of organismal complexity increases with colony size in eusocial species similar to the increase of complexity with size that has been shown for the whole range of living organisms. We show that queen and worker lifespan diverge in closely related species representing the transition from solitary to social life and show that queen and worker lifespan are correlated if colony size is taken into account: with increasing colony size the lifespan differential between queen and worker increases, whereas neither queen nor worker lifespan is associated with colony size. Additionally, the lifespan differential is better explained by colony size than by the weight differences between the castes. The divergence of phenotypes found is in line with the increasing specialization of subunits in larger organisms, which leads to increasing complexity. We argue that division of labour is acting to increase colony efficiency, which in turn shapes the investments made into individuals leading to short‐lived workers and long‐lived queens. Additionally, maintenance investments may be shaped due to the variable extrinsic risk faced by different castes. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 710–724.     

What is “phenoptosis” and how to fight it?

Phenoptosis is the death of an organism programmed by its genome. Numerous examples of phenoptosis are described in prokaryotes, unicellular eukaryotes, and all kingdoms of multicellular eukaryotes (animals, plants, and fungi). There are very demonstrative cases of acute phenoptosis when actuation of a specific biochemical or behavioral program results in immediate death. Rapid (taking days) senescence of semelparous plants is described as phenoptosis controlled by already known genes and mediated by toxic phytohormones like abscisic acid. In soya, the death signal is transmitted from beans to leaves via xylem, inducing leaf fall and death of the plant. Mutations in two genes of Arabidopsis thaliana, required for the flowering and subsequent formation of seeds, prevent senescence, strongly prolonging the lifespan of this small semelparous grass that becomes a big bush with woody stem, and initiate substitution of vegetative for sexual reproduction. The death of pacific salmon immediately after spawning is surely programmed. In this case, numerous typical traits of aging, including amyloid plaques in the brain, appear on the time scale of days. There are some indications that slow aging of higher animals and humans is also programmed, being the final step of ontogenesis. It is assumed that stepwise decline of many physiological functions during such aging increases pressure of natural selection on organisms stimulating in this way biological evolution. As a working hypothesis, the biochemical mechanism of slow aging is proposed. It is assumed that mitochondria-generated reactive oxygen species (ROS) is a tool to stimulate apoptosis, an effect decreasing with age the cell number (cellularity) of organs and tissues. A group of SkQ-type substances composed of plastoquinone and a penetrating cation were synthesized to target an antioxidant into mitochondria and to prevent the age-linked rise of the mitochondrial ROS level. Such targeting is due to the fact that mitochondria are the only cellular organelles that are negatively charged compared to the cytosol. SkQs are shown to strongly decrease concentration of ROS in mitochondria, prolong lifespan of fungi, invertebrates, fish, and mammals, and retard appearance of numerous traits of aging. Clinical trials of SkQ1 (plastoquinonyl decyltriphenylphosphonium) have been successfully completed so that the Ministry of Health of the Russian Federation recommends drops of very dilute (0.25 μM) solution of this antioxidant as a medicine to treat the syndrome of dry eye, which was previously considered an incurable disease developing with age. These drops are already available in drugstores. Thus, SkQ1 is the first mitochondria-targeted drug employed in medical practice.     

Stress resistance and longevity are not directly linked to levels of enzymatic antioxidants in the ponerine ant Harpegnathos saltator

Background

The molecular mechanisms of variations in individual longevity are not well understood, even though longevity can be increased substantially by means of diverse experimental manipulations. One of the factors supposed to be involved in the increase of longevity is a higher stress resistance. To test this hypothesis in a natural system, eusocial insects such as bees or ants are ideally suited. In contrast to most other eusocial insects, ponerine ants show a peculiar life history that comprises the possibility to switch during adult life from a normal worker to a reproductive gamergate, therewith increasing their life expectancy significantly.

Results

We show that increased resistance against major stressors, such as reactive oxygen species and infection accompanies the switch from a life-history trait with normal lifespan to one with a longer life expectancy. A short period of social isolation was sufficient to enhance stress resistance of workers from the ponerine ant species Harpegnathos saltator significantly. All ant groups with increased stress resistances (reproducing gamergates and socially isolated workers) have lower catalase activities and glutathione levels than normal workers. Therewith, these ants resemble the characteristics of the youngest ants in the colony.

Conclusions

Social insects with their specific life history including a switch from normal workers to reproducing gamergates during adult life are well suited for ageing research. The regulation of stress resistance in gamergates seemed to be modified compared to foraging workers in an economic way. Interestingly, a switch towards more stress resistant animals can also be induced by a brief period of social isolation, which may already be associated with a shift to a reproductive trajectory. In Harpegnathos saltator, stress resistances are differently and potentially more economically regulated in reproductive individuals, highlighting the significance of reproduction for an increase in longevity in social insects. As already shown for other organisms with a long lifespan, this trait is not directly coupled to higher levels of enzymatic and non-enzymatic antioxidants.     

The disposable soma theory revisited: Time as a resource in the theories of aging

All life processes are subject to time constraints. At the cellular level, damage repair and cell cycle arrest are interrelated, allowing sufficient time for repair prior to cell cycle progression. Organisms have evolved so that developmental timing is linked to environmental conditions, such as nutrient availability and predation. Recent results in mammals regarding species-specific differences in cell cycle arrest and DNA damage suggest that a stable cell cycle arrest is a feature of longer-lived species. The implication of these results is that longer-lived species delay cell cycle progression to a greater degree than shorter-lived species, allowing for higher fidelity repair. We suggest that the ability to devote longer periods of time to repair and maintenance is a key feature of longer-lived species, and that evolutionary pressure to complete repair and resume cell division is a determinant of species lifespan. Thus, time is a resource that must be managed by the organism to attempt to maximize the fidelity of repair while completing development and reproduction in the limited window of opportunity afforded by environmental pressures. This viewpoint on time as a resource has implications for theories regarding the aging process and the development of species lifespan.     

On the cause and mechanism of phenoptosis

Based upon evolvability theory, phenotypes like aging that offer no apparent individual benefit may evolve nonetheless. Pursuant to that concept, the evolution of a hypothetical, genome-based aging program called phenoptosis was proposed. However, while aging may facilitate evolvability, it need not result from a program specifically selected for that purpose. Instead, it is possible that the potential for aging is conserved within the genome as a part of a beneficial program that orchestrates and integrates developmental transformation of the soma from conception to maturation. Because somatic remodeling is inherently unstable, its continued non-programmatic expression beyond young adulthood (developmental inertia) erodes internal order, initiating and exacerbating aging. Thus, aging may result paradoxically from post-maturational expression of the same programmatic function for somatic transformation that previously provided individual benefit. It did so by ensuring acquisition of reproductive competence, post-reproductive development of parents to nurture offspring and thereby, to guarantee species survival. In an attempt to identify genes capable of controlling developmental inertia, we sequenced DNA from a series of subjects displaying extreme neoteny, i.e. retention of youthful characteristics during adulthood. We hoped to identify mutations associated with delayed development and to compare each subject’s biological and chronological ages. De novo mutations of coding-genes were found in all the subjects, but they could not be definitively identified as a cause of developmental delay. Nonetheless, genetic and epigenetic studies of neotenic subject’s DNA are on-going. We are attempting to determine if phenoptosis specifically evolved to cause aging, or rather if it exists as a cryptic component of the developmental program that expresses its lethal potential serendipitously and only after individual benefit is realized.     

Insights into the structure of plant-insect communities: Specialism and generalism in a regional set of non-pollinating fig wasp communities

Insects show a multitude of symbiotic interactions that may vary in degree of specialization and structure. Gall-inducing insects and their parasitoids are thought to be relatively specialized organisms, but despite their ecological importance, the organization and structure of the interactions they establish with their hosts has seldom been investigated in tropical communities. Non-pollinating fig wasps (NPFW) are particularly interesting organisms for the study of ecological networks because most species strictly develop their offspring within fig inflorescences, and show a multitude of life history strategies. They can be gall-makers, cleptoparasites or parasitoids of pollinating or of other non-pollinating fig wasps. Here we analysed a set of non-pollinating fig wasp communities associated with six species of Ficus section Americanae over a wide area. This allowed us to investigate patterns of specialization in a diverse community composed of monophagous and polyphagous species. We observed that most NPFW species were cleptoparasites and parasitoids, colonizing figs several days after oviposition by pollinators. Most species that occurred in more than one host were much more abundant in a single preferential host, suggesting specialization. The food web established between wasps and figs shows structural properties that are typical of specific antagonistic relationships, especially of endophagous insect networks. Two species that occurred in all available hosts were highly abundant in the network, suggesting that in some cases generalized species can be more competitive than strict specialists. The Neotropical and, to a lesser extent, Afrotropical NPFW communities seem to be more generalized than other NPFW communities. However, evidence of host sharing in the Old World is quite limited, since most studies have focused on particular taxonomic groups (genera) of wasps instead of sampling the whole NPFW community. Moreover, the lack of quantitative information in previous studies prevents us from detecting patterns of host preferences in polyphagous species.     

Degrees of disruption: projected temperature increase has catastrophic consequences for reproduction in a tropical ectotherm

Although climate change models predict relatively modest increases in temperature in the tropics by the end of the century, recent analyses identify tropical ectotherms as the organisms most at risk from climate warming. Because metabolic rate in ectotherms increases exponentially with temperature, even a small rise in temperature poses a physiological threat to tropical ectotherms inhabiting an already hot environment. If correct, the metabolic theory of climate warming has profound implications for global biodiversity, since tropical insects and arachnids constitute the vast majority of animal species. Predicting how climate change will translate into fitness consequences for tropical arthropods requires an understanding of the effects of temperature increase on the entire life history of the species. Here, in a comprehensive case study of the fitness consequences of the projected temperature increase for the tropics, we conducted a split‐brood experiment on the neotropical pseudoscorpion, Cordylochernes scorpioides, in which 792 offspring from 33 females were randomly assigned at birth to control‐ and high‐temperature treatments for rearing through the adult stage. The diurnally varying, control treatment temperature was determined from long‐term, average daily temperature minima and maxima in the pseudoscorpion's native habitat. In the high temperature treatment, increasing temperature by the 3.5 °C predicted for the tropics significantly reduced survival and accelerated development at the cost of reduced adult size and a dramatic decrease in level of sexual dimorphism. The most striking effects, however, involved reproductive traits. Reared at high temperature, males produced 45% as many sperm as control males, and females failed to reproduce. Sequencing of the mitochondrial ND2 gene revealed two highly divergent haplogroups that differed substantially in developmental rate and survivorship but not in reproductive response to high temperature. Our findings suggest that reproduction may be the Achilles’ heel of tropical ectotherms, as climate warming subjects them to an increasingly adverse thermal environment.     

Biodemographic analysis of male honey bee mortality

Biodemographic studies of insects have significantly enhanced our understanding of the biology of aging. Eusocial insects have evolved to form different groups of colony members that are specialized for particular tasks and highly dependent on each other. These different groups (castes and sexes) also differ strongly in their life expectancy but relatively little is known about their mortality dynamics. In this study we present data on the age-specific flight activity and mortality of male honey bees from two different genetic lines that are exclusively dedicated to reproduction. We show that males initiating flight at a young age experience more flight events during their lifetime. No (negative) relation between the age at flight initiation and lifespan exists, as might be predicted on the basis of the antagonistic pleiotropy theory of aging. Furthermore, we fit our data to different aging models and conclude that overall a slight deceleration of the age-dependent mortality increase at advanced ages occurs. However, mortality risk increases according to the Gompertz-Makeham model when only days with flight activity (active days) are taken into account. Our interpretation of the latter is that two mortality components act on honey bee males during flight: increasing, age-dependent deaths (possibly from wear-and-tear), and age-independent deaths (possibly due to predation). The overall mortality curve is caused by the interaction of the distribution of age at foraging initiation and the mortality function during the active (flight) lifespan.     

Two-sex life table of Nasonia vitripennis (Hymenoptera: Pteromalidae) and the effects of Wolbachia on its reproduction and parasitism of Musca domestica (Diptera: Muscidae)

Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) is now emerging as genetic model organism for development and genetics research. As a parasitic insect, the egg, larval, pupal, and early adult developmental stages of N. vitripennis occur within the enclosed fly pupae, which differ a lot from the life cycle of other insects that undergo complete metamorphosis. Previous report on the life table of N. vitripennis was based on females only. In this study, the two-sex life table approach was used to examine the parasitic efficiency of N. vitripennis within the pupae of Musca domestica L. (Diptera: Muscidae), and the influence of low temperature and the endosymbiotic bacteria Wolbachia on wasp population growth were investigated. Wolbachia could improve the fecundity of N. vitripennis and prolong the host life history. We propose the preservation of M. domestica pupae at 4 °C for 15 days is suitable in practical use. Age-stage, two-sex life table analysis revealed the stage structure and variability of N. vitripennis population growth, and also provide useful information about the effects of Wolbachia on its reproduction and parasitism of M. domestica.     

Why grow up? A perspective on insect strategies to avoid metamorphosis

1. Insects with complete metamorphosis (holometaboly) are extremely successful, constituting over 60% of all described animal species. Complete metamorphosis confers significant advantages because it enables organisms to optimise life‐history components through temporal partitioning, and thereby to exploit multiple ecological niches. Yet holometaboly can also impose costs, and several lineages have evolved life cycle modifications to avoid complete metamorphosis. 2. In this review, we discuss different strategies that have evolved that result in the loss of complete metamorphosis (type I and type II paedomorphosis). In addition, the ecological pressures and developmental modifications that facilitate this avoidance are considered, as well as the importance of life cycle complexity in life‐history evolution. 3. Interestingly, only female holometabolous insects have entirely avoided complete metamorphosis, and it is always the ancestrally juvenile morphology that is retained. These findings point to a strong sex‐biased trade‐off between investment in reproduction and development. While the loss of complete metamorphosis in females has occurred independently on several occasions across holometabolous insects, only a small number of species possessing this ability have been described. 4. Thus, complete metamorphosis, which originated only once in insects, appears to have been almost fully retained. This indicates that significant modifications to the holometabolan metamorphic ground plan are highly constrained, and suggests that the transition to complete metamorphosis is evolutionarily irreversible.     

Effect of food restriction on survival and reproduction of a termite

Food availability affects the trade-off between maintenance and reproduction in a wide range of organisms, but its effects on social insects remain poorly understood. In social insects, the maintenance-reproduction trade-off seems to be absent in individuals but may appear at the colony level, although this is rarely investigated. In this study, we restricted food availability in a termite species to test how it affects survival and reproduction, both at the individual and colony level. Using Bayesian multivariate response models, we found very minor effects of food restriction on the survival of queens, individual workers or on the colonies. In contrast, queen fecundity was significantly reduced, whereas colony-level fecundity (i.e., the number of dispersing alates, future reproductives) increased under food restriction as workers gave up cooperation within the colony and became alates that dispersed. Our study shows that life-history trade-offs can be mitigated by individuals' social behaviours in social organisms.     

Long life cycles in insects

Long life cycles covering more than one year are known for all orders of insects. There are different mechanisms of prolongation of the life cycle: (1) slow larval development; (2) prolongation of the adult stage with several reproduction periods; (3) prolongation of diapause; (4) combination of these mechanisms in one life cycle. Lasting suboptimal conditions (such as low temperature, low quality of food or instability of food resources, natural enemies, etc.) tend to prolong life cycles of all individuals in a population. In this case, the larvae feed and develop for longer than a year, and the active periods are interrupted by dormancy periods. The nature of this dormancy is unknown: in some cases it appears to be simple quiescence, in others it has been experimentally shown to be a true diapause. Induction and termination of these repeated dormancy states are controlled by different environmental cues, the day-length being the principal one as in the case of the annual diapause. The long life cycles resulting from prolonged adult lifespan were experimentally studied mainly in beetles and true bugs. The possibility of repeated diapause and several periods of reproductive activity is related to the fact that the adults remain sensitive to day length, which is the main environmental cue controlling their alternative physiological states (reproduction vs. diapause). Habitats with unpredictable environmental changes stimulate some individuals in a population to extend their life cycles by prolonged diapause. The properties of this diapause are poorly understood, but results of studies of a few species suggest that this physiological state differs from the true annual diapause in deeper suppression of metabolism. Induction and intensity of prolonged diapause in some species appear to be genetically controlled, so that the duration of prolonged diapause varies among individuals in a group, even that of sibles reared under identical conditions. Thus, long life cycles are realized due to the ability of insects to interrupt activity repeatedly and enter dormancy. This provides high resistance to various environmental factors. Regardless of the nature of this dormancy (quiescence, annual or prolonged diapause, or other forms) and the life cycle duration, the adults always appear synchronously after dormancy in the nature. The only feasible explanation of this is the presence of a special synchronizing mechanism, most likely both exo- and endogenous, since the adults appear not only synchronously but also in the period best suited for reproduction. As a whole, the long life cycles resulting from various structural modifications of the annual life cycle, are typical of the species living under stable suboptimal conditions when the pressure of individual environmental factors is close to the tolerance limits of the species, even though it represents its norm of existence. Such life cycles are also typical of the insects living in unstable environments with unpredictable variability of conditions, those developing in cones and galls, feeding on flowers, seeds, or fruits with limited periods of availability, those associated with the plant species with irregular patterns of blossoming and fruiting, and those consuming low-quality food or depending on unpredictable food sources (e.g., predators or parasites). Long cycles are more common in: (1) insect species at high latitudes and mountain landscapes where the vegetation season is short and unstable; (2) species living in deserts or arid areas where precipitation is unstable and often insufficient for survival of food plants; (3) inhabitants of cold and temporary water bodies that are not filled with water every year. At the same time, long life cycles sometimes occur in insects from other climatic zones as well. It is also important to note that while there is a large body of literature dealing with the long life cycles in insects, it mostly focuses on external aspects of the phenomenon. Experimental studies are needed to understand this phenomenon, first of all the nature of dormancy and mechanisms of synchronization of adult emergence.     

Per-capita productivity in a social wasp: no evidence for a negative effect of colony size

Optimal colony size in eusocial insects likely reflects a balance between ecological factors and factors intrinsic to the social group. In a seminal paper Michener (1964) showed for some species of social Hymenoptera that colony production of immature stages (productivity), when transformed to a per-female basis, was inversely related to colony size. He concluded that social patterns exist in the social insects that cause smaller groups to be more efficient than larger groups. This result has come to be known as “Michener’s paradox” because it suggests that selection on efficiency would oppose the evolution of the large and complex societies that are common in the social insects. Michener suggested that large colony size has other advantages, such as improved defense and homeostasis, that are favored by selection. For his analysis of swarm-founding wasps, Michener combined data from colonies of different species and different developmental stages in order to obtain adequate sample sizes; therefore, his study did not make a strong case that efficiency decreases with increasing colony size (across colonies) in these wasps. We tested Michener’s hypothesis on the Neotropical swarm-founding wasp Parachartergus fraternus, while controlling for stage of colony development. We found that small colonies were more variable in percapita productivity relative to larger colonies, but found no evidence for a negative relationship between efficiency and size across colonies. Received 1 February 2006; revised 5 May 2006; accepted 11 May 2006.     

Ant Colonies Do Not Trade-Off Reproduction against Maintenance

The question on how individuals allocate resources into maintenance and reproduction is one of the central questions in life history theory. Yet, resource allocation into maintenance on the organismic level can only be measured indirectly. This is different in a social insect colony, a “superorganism” where workers represent the soma and the queen the germ line of the colony. Here, we investigate whether trade-offs exist between maintenance and reproduction on two levels of biological organization, queens and colonies, by following single-queen colonies of the ant Cardiocondyla obscurior throughout the entire lifespan of the queen. Our results show that maintenance and reproduction are positively correlated on the colony level, and we confirm results of an earlier study that found no trade-off on the individual (queen) level. We attribute this unexpected outcome to the existence of a positive feedback loop where investment into maintenance (workers) increases the rate of resource acquisition under laboratory conditions. Even though food was provided ad libitum, variation in productivity among the colonies suggests that resources can only be utilized and invested into additional maintenance and reproduction by the colony if enough workers are available. The resulting relationship between per-capita and colony productivity in our study fits well with other studies conducted in the field, where decreasing per-capita productivity and the leveling off of colony productivity have been linked to density dependent effects due to competition among colonies. This suggests that the absence of trade-offs in our laboratory study might also be prevalent under natural conditions, leading to a positive association of maintenance, (= growth) and reproduction. In this respect, insect colonies resemble indeterminate growing organisms.     

Comparative idiosyncrasies in life extension by reduced mTOR signalling and its distinctiveness from dietary restriction

Reduced mechanistic target of rapamycin (mTOR) signalling extends lifespan in yeast, nematodes, fruit flies and mice, highlighting a physiological pathway that could modulate aging in evolutionarily divergent organisms. This signalling system is also hypothesized to play a central role in lifespan extension via dietary restriction. By collating data from 48 available published studies examining lifespan with reduced mTOR signalling, we show that reduced mTOR signalling provides similar increases in median lifespan across species, with genetic mTOR manipulations consistently providing greater life extension than pharmacological treatment with rapamycin. In contrast to the consistency in changes in median lifespan, however, the demographic causes for life extension are highly species specific. Reduced mTOR signalling extends lifespan in nematodes by strongly reducing the degree to which mortality rates increase with age (aging rate). By contrast, life extension in mice and yeast occurs largely by pushing back the onset of aging, but not altering the shape of the mortality curve once aging starts. Importantly, in mice, the altered pattern of mortality induced by reduced mTOR signalling is different to that induced by dietary restriction, which reduces the rate of aging. Effects of mTOR signalling were also sex dependent, but only within mice, and not within flies, thus again species specific. An alleviation of age‐associated mortality is not a shared feature of reduced mTOR signalling across model organisms and does not replicate the established age‐related survival benefits of dietary restriction.     

Reproductive competence: a recurrent logic module in eukaryotic development

Developmental competence is the ability to differentiate in response to an appropriate stimulus, as first elaborated by Waddington in relation to organs and tissues. Competence thresholds operate at all levels of biological systems from the molecular (e.g. the cell cycle) to the ontological (e.g. metamorphosis and reproduction). Reproductive competence, an organismal process, is well studied in mammals (sexual maturity) and plants (vegetative phase change), though far less than later stages of terminal differentiation. The phenomenon has also been documented in multiple species of multicellular fungi, mostly in early, disparate literature, providing a clear example of physiological differentiation in the absence of morphological change. This review brings together data on reproductive competence in Ascomycete fungi, particularly the model filamentous fungus Aspergillus nidulans, contrasting mechanisms within Unikonts and plants. We posit reproductive competence is an elementary logic module necessary for coordinated development of multicellular organisms or functional units. This includes unitary multicellular life as well as colonial species both unicellular and multicellular (e.g. social insects such as ants). We discuss adaptive hypotheses for developmental and reproductive competence systems and suggest experimental work to address the evolutionary origins, generality and genetic basis of competence in the fungal kingdom.     

Cost-free lifespan extension via optimization of gene expression in adulthood aligns with the developmental theory of ageing

Ageing evolves because the force of selection on traits declines with age but the proximate causes of ageing are incompletely understood. The ‘disposable soma’ theory of ageing (DST) upholds that competitive resource allocation between reproduction and somatic maintenance underpins the evolution of ageing and lifespan. In contrast, the developmental theory of ageing (DTA) suggests that organismal senescence is caused by suboptimal gene expression in adulthood. While the DST predicts the trade-off between reproduction and lifespan, the DTA predicts that age-specific optimization of gene expression can increase lifespan without reproduction costs. Here we investigated the consequences for lifespan, reproduction, egg size and individual fitness of early-life, adulthood and post-reproductive onset of RNAi knockdown of five ‘longevity’ genes involved in key biological processes in Caenorhabditis elegans. Downregulation of these genes in adulthood and/or during post-reproductive period increases lifespan, while we found limited evidence for a link between impaired reproduction and extended lifespan. Our findings demonstrate that suboptimal gene expression in adulthood often contributes to reduced lifespan directly rather than through competitive resource allocation between reproduction and somatic maintenance. Therefore, age-specific optimization of gene expression in evolutionarily conserved signalling pathways that regulate organismal life histories can increase lifespan without fitness costs.