The life history of Formica exsecta (Hymenoptera : Formicidae) from an ecological and evolutionary perspective

With their sedentary colonies, long-lived ant colonies lend themselves to long-term studies where fitness effects of life-history traits can be investigated in the wild, a task that is challenging in any organism and particularly rarely feasible in insects. Here, we summarize and examine the insights we have gained from a 28-year study on monogyne colonies of the narrow-headed ant Formica exsecta NYLANDER, 1846, and discuss the ecological and genetic repercussions that emanate from ecological realities and conflicting selection pressures in a fragmented landscape matrix. These entail the effects of habitat structuration on genetic diversity, the effects of reduced genetic diversity on the fitness of individuals and colonies, and the impact of the opposing selection pressures on short-versus long-range dispersal.Peer reviewe

Sisäsiitoksen syyt ja seuraukset loviniskamuurahaisella

Human actions cause destruction and fragmentation of natural habitats, predisposing populations to loss of genetic diversity and inbreeding, which may further decrease their fitness and survival. Understanding these processes is a main concern in conservation genetics. Yet data from natural populations is scarce, particularly on invertebrates, owing to difficulties in measuring both fitness and inbreeding in the wild. Ants are social insects, and a prime example of an ecologically important group for which the effects of inbreeding remain largely unstudied. Social insects serve key roles in all terrestrial ecosystems, and the division of labor between the females in the colonies queens reproduce, workers tend to the developing brood probably is central to their ecological success. Sociality also has important implications for the effects of inbreeding. Despite their relative abundance, the effective population sizes of social insects tend to be small, owing to the low numbers of reproductive individuals relative to the numbers of sterile workers. This may subject social insects to loss of genetic diversity and subsequent inbreeding depression. Moreover, both the workers and queens can be inbred, with different and possibly multiplicative consequences. The aim of this study was to investigate causes and consequences of inbreeding in a natural population of ants. I used a combination of long-term field and genetic data from colonies of the narrow-headed ant Formica exsecta to examine dispersal, mating behavior and the occurrence of inbreeding, and its consequences on individual and colony traits. Mating in this species takes place in nuptial flights that have been assumed to be population-wide and panmictic. My results, however, show that dispersal is local, with queens establishing new colonies as close as 60 meters from their natal colony. Even though actual sib-mating was rare, individuals from different but related colonies pair, which causes the population to be inbred. Furthermore, multiple mates of queens were related to each other, which also indicates localized mating flights. Hence, known mechanisms of inbreeding avoidance, dispersal and multiple mating, were not effective in this population, as neither reduced inbreeding level of the future colony. Inbreeding had negative consequences both at the individual and colony level. A queen that has mated with a related male produces inbred workers, which impairs the colony s reproductive success. The inbred colonies were less productive and, specifically, produced fewer new queens, possibly owing to effects of inbreeding on the caste determination of female larvae. A striking finding was that males raised in colonies with inbred workers were smaller, which reflects an effect of the social environment as males, being haploid, cannot be inbred themselves. The queens produced in the inbred colonies, in contrast, were not smaller, but their immune response was up-regulated. Inbreeding had no effect on queen dispersal, but inbred queens had a lower probability of successfully founding a new colony. Ultimately, queens that survived through the colony founding phase had a shorter lifespan. This supports the idea that inbreeding imposes a genetic stress, leading to inbreeding depression on both the queen and the colony level. My results show that inbreeding can have profound consequences on insects in the wild, and that in social species the effects of inbreeding may be multiplicative and mediated through the diversity of the social environment, as well as the genetic makeup of the individuals themselves. This emphasizes the need to take into account all levels of organization when assessing the effects of genetic diversity in social animals.Ihmisen toimet aiheuttavat luontaisten elinympäristöjen häviämistä ja pirstoutumista. Tämän seurauksena eläinten populaatiokoot pienenevät, ja niiden leviäminen alueelta toiselle voi estyä, ja sisäsiitos, eli pariutuminen sukulaisten kanssa, voi yleistyä. Sisäsiitos puolestaan heikentää yksilöiden elinkykyä ja kelpoisuutta ja mahdollisesti vaarantaa ennestään pienentyneitä kantoja. Sisäsiitoksen vaikutukset luonnossa tunnetaan kuitenkin puutteellisesti varsinkin selkärangattomilla eläimillä, sillä sisäsiitoksen ja sen vaikutusten mittaaminen luonnonoloissa on haasteellista. Muurahaiset ovat yhteiskuntahyönteisiä ja ekologisesti hyvin merkittävä ja runsas eläinryhmä. Niiden menestys perustuu tehokkaaseen lisääntymistyönjakoon naaraiden välillä: kuningattaret lisääntyvät, ja työläiset hoitavat jälkeläiset. Vaikka työläisiä olisi runsaastikin, lisääntyviä yksilöitä voi työnjaosta johtuen olla hyvin vähän, mikä voi altistaa muurahaisia sisäsiitoksen vaikutuksille. Muurahaiskuningattaren pariutumiskäyttäytymisellä on lisäksi kauaskantoiset seuraukset, sillä se parittelee elämänsä aikana vain kerran. Sen jälkeen se perustaa pesän ja voi elää vuosikymmeniä tuottaen jälkeläisiä varastoimiensa siittiöiden avulla. Muurahaispesässä on kaksi sukupolvea, joista molemmat voivat olla sisäsiittoisia: kuningatar, jos sen vanhemmat ovat sukua keskenään, ja pesän työläisjälkeläiset, jos kuningatar on paritellut lähisukuisen koiraan kanssa ennen pesän perustamista. Tutkin väitöskirjatyössäni sisäsiitoksen syitä ja seurauksia loviniskamuurahaisen luonnonpesissä Tvärminnen eläintieteellisellä asemalla Hangossa. Käytin työssäni pitkäaikaista seuranta-aineistoa muurahaispesien tuottavuudesta ja geneettisestä taustasta tutkiakseni muurahaisten leviämiskäyttäytymistä sekä sisäsiitoksen yleisyyttä ja vaikutuksia yksilön ja pesän tasolla. Muurahaisten häälentojen on oletettu olevan tehokas tapa vähentää sisäsiitosta, mutta tutkimuksessa kävi ilmi, että lentoetäisyydet olivat hyvin lyhyitä ja sisäsiitos yleistä. Kuningattaret pariutuivat lähisukuisten, joskaan eivät tavallisesti niiden omasta kotipesästä tulevien koiraiden kanssa, ja perustivat uuden pesän keskimäärin vain 60 metrin päähän kotipesästään. Pitempi lentomatka ei vähentänyt kuningattaren riskiä pariutua lähisukulaisen kanssa. Kuningattaret eivät myöskään voineet lieventää sisäsiitoksen vaikutuksia parittelemalla useiden koiraiden kanssa, sillä koiraat olivat usein sukua keskenään. Sisäsiitoksella oli monenlaisia haittavaikutuksia. Sisäsiittoiset työläiset olivat tehottomampia kasvattamaan uusia yksilöitä, mikä heikensi pesän lisääntymismenestystä. Mielenkiintoinen havainto oli, että sisäsiittoiset pesät tuottivat pienikokoisempia koirasjälkeläisiä, mikä johtuu nimenomaan niitä hoitavien työläisten sisäsiitosheikkoudesta. Koiraat itse eivät voi olla sisäsiittoisia, sillä ne syntyvät hedelmöitymättömistä munista. Sisäsiittoiset pesät myös tuottivat vähemmän uusia kuningattaria, ja niistä tulevilla kuningattarilla oli kohonnut immuunivaste. Uuden pesän perustaminen on energiaa vaativa elämänvaihe, jossa kohonnut immuunivaste voi olla ylimääräinen rasite. Sisäsiitos heikensikin kuningatarten pesänperustusmenestystä. Sisäsiitos ei vaikuttanut kuningatarten leviämiskykyyn, mutta sisäsiittoiset kuningattaret olivat taipuvaisempia itse pariutumaan sukulaisten kanssa ja elivät lyhyemmän aikaa. Tutkimukseni osoittaa, että sisäsiitoksella on vaikutuksia kaikissa muurahaispesän elinkaaren vaiheissa, ja nämä vaikutukset kertautuvat sekä työläisten että kuningatarten kautta

Causes and consequences of intergroup conflict in cooperative banded mongooses

This is the final version of the article. Available from Elsevier Masson via the DOI in this record.Conflict between groups is a notable feature of many animal societies. Recent theoretical models suggest that violent intergroup conflict can shape patterns of within-group cooperation. However, despite its prevalence in social species, the adaptive significance of violent intergroup conflict has been little explored outside of humans and chimpanzees, Pan troglodytes. A barrier to current understanding of the role of intergroup conflict in the evolution of social behaviour is a lack of information on the causes and consequences of aggression between groups. Here, we examined the causes and fitness consequences of intergroup conflict in the banded mongoose, Mungos mungo, using a 16-year data set of observed intergroup interactions, life history and behaviour. Banded mongooses are cooperative breeders that live in highly territorial groups and engage in frequent, aggressive and violent intergroup interactions. We found that intensified population-wide competition for food and mates increased the probability of intergroup interactions, and that increased intergroup conflict was associated with periods in which groups were growing in size. Intergroup conflict had fitness costs in terms of reduced litter and adult survival but no cost to pregnant females: in fact, females were less likely to abort following an intergroup interaction than when there had been no recent intergroup conflict. Our results suggest that intergroup conflict has measurable costs to both individuals and groups in the long and short term, and that levels of conflict among groups could be high enough to affect patterns of within-group cooperative behaviour. Establishing the consequences of intergroup conflict in cooperative species can shed light on patterns of conflict and cooperation within groups and, in turn, facilitate our understanding of social evolution.Funding was provided by a Natural Environment Research Council grant no. NE/J010278/1 to M.A.C. and a European Research Council grant no. 309249 to M.A.C

Live long and prosper : durable benefits of early-life care in banded mongooses

Kin selection theory defines the conditions for which altruism or 'helping' can be favoured by natural selection. Tests of this theory in cooperatively breeding animals have focused on the short-term benefits to the recipients of help, such as improved growth or survival to adulthood. However, research on early-life effects suggests that there may be more durable, lifelong fitness impacts to the recipients of help, which in theory should strengthen selection for helping. Here, we show in cooperatively breeding banded mongooses (Mungos mungo) that care received in the first 3 months of life has lifelong fitness benefits for both male and female recipients. In this species, adult helpers called 'escorts' form exclusive one-to-one caring relationships with specific pups (not their own offspring), allowing us to isolate the effects of being escorted on later reproduction and survival. Pups that were more closely escorted were heavier at sexual maturity, which was associated with higher lifetime reproductive success for both sexes. Moreover, for female offspring, lifetime reproductive success increased with the level of escorting received per se, over and above any effect on body mass. Our results suggest that early-life social care has durable benefits to offspring of both sexes in this species. Given the well-established developmental effects of early-life care in laboratory animals and humans, we suggest that similar effects are likely to be widespread in social animals more generally. We discuss some of the implications of durable fitness benefits for the evolution of intergenerational helping in cooperative animal societies, including humans. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.Peer reviewe

Natal dispersal, mating patterns and inbreeding in the ant Formica exsecta

Peer reviewe

Developing differences: early-life effects and evolutionary medicine

Variation in early-life conditions can trigger developmental switches that lead to predictable individual differences in adult behaviour and physiology. Despite evidence for such early-life effects being widespread both in humans and throughout the animal kingdom, the evolutionary causes and consequences of this developmental plasticity remain unclear. The current issue aims to bring together studies of early-life effects from the fields of both evolutionary ecology and biomedicine to synthesise and advance current knowledge of how information is used during development, the mechanisms involved, and how early-life effects evolved. We hope this will stimulate further research into early-life effects, improving our understanding of why individuals differ and how this might influence their susceptibility to disease. This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine’.</p

Lack of aggression and apparent altruism towards intruders in a primitive termite

This is the author accepted manuscript. The final version is available from Royal Society via the DOI in this record.In eusocial insects, the ability to discriminate nestmates from non-nestmates is widespread and ensures that altruistic actions are directed towards kin and agonistic actions are directed towards non-relatives. Most tests of nestmate recognition have focused on hymenopterans, and suggest that cooperation typically evolves in tandem with strong antagonism towards non-nestmates. Here we present evidence from a phylogenetically and behaviourally basal termite species that workers discriminate members of foreign colonies. However, contrary to our expectations, foreign intruders were the recipients of more rather than less cooperative behaviour, and were not subjected to elevated aggression. We suggest that relations between groups may be much more peaceable in basal termites compared to eusocial hymenoptera, owing to energetic and temporal constraints on colony growth, and the reduced incentive that totipotent workers (who may inherit breeding status) have to contribute to self-sacrificial intergroup conflict.The research was supported by a Royal Society University Research Fellowship (to MAC)

Telomere dynamics in wild banded mongooses: Evaluating longitudinal and quasi-longitudinal markers of senescence

This is the author accepted manuscript. The final version is available from Elsevier via the DOI in this record.Telomere length and the rate of telomere shortening have been suggested as particularly useful physiological biomarkers of the processes involved in senescent decline of somatic and reproductive function. However, longitudinal data on changes in telomere length across the lifespan are difficult to obtain, particularly for long-lived animals. Quasi-longitudinal studies have been proposed as a method to gain insight into telomere dynamics in long-lived species. In this method, minimally replicative cells are used as the baseline telomere length against which telomere length in highly replicative cells (which represent the current state) can be compared. Here we test the assumptions and predictions of the quasi-longitudinal approach using longitudinal telomere data in a wild cooperative mammal, the banded mongoose, Mungos mungo. Contrary to our prediction, telomere length (TL) was longer in leukocytes than in ear cartilage. Longitudinally, the TL of ear cartilage shortened with age, but there was no change in the TL of leukocytes, and we also observed many individuals in which TL increased rather than decreased with age. Leukocyte TL but not cartilage TL was a predictor of total lifespan, while neither predicted post-sampling survival. Our data do not support the hypothesis that cross-tissue comparison in TL can act as a quasi-longitudinal marker of senescence. Rather, our results suggest that telomere dynamics in banded mongooses are more complex than is typically assumed, and that longitudinal studies across whole life spans are required to elucidate the link between telomere dynamics and senescence in natural populations.The research was funded by a European Research Council Consolidator’s Grant (no. 309249) to MAC and a Natural Environment Research Council (UK) Standard Grant (NE/G019657/1) to MAC and JDB

Maternal stress or sleep during pregnancy are not reflected on telomere length of newborns

Telomeres play an important role in maintaining chromosomal integrity.With each cell division, telomeres are shortened and leukocyte telomere length (LTL) has therefore been considered a marker for biological age. LTL is associated with various lifetime stressors and health‑related outcomes. Transgenerationaleffects have been implicated in newborns, with maternal stress, depression,and anxiety predicting shorter telomere length at birth, possibly reflecting the intrauterine growth environment. Previous studies, with relatively small sample sizes, have reported an effect of maternal stress, BMI, and depression during pregnancy on the LTL of newborns. Here, we attempted to replicate previous findings on prenatal stress and newborn LTL in a sample of 1405 infants using aqPCR‑based method.In addition, previous research has been expanded by studying the relationship between maternal sleep quality and LTL. Maternal prenatal stress, anxiety, depression, BMI, and self‑reported sleep quality were evaluated with self‑reported questionnaires.Despite sufficient power to detect similar or even considerably smaller effects than those previously reported in the literature,we were unable to replicate the previous correlation between maternal stress, anxiety, depression,or sleep with LTL. We discuss several possible reasons for the discrepancies between our findings and those previously described.Peer reviewe