0000000000587386
AUTHOR
Evelien Jongepier
Parasite presence induces gene expression changes in an ant host related to immunity and longevity
Most species are either parasites or exploited by parasites, making parasite&ndash
Insect societies fight back: the evolution of defensive traits against social parasites
Insect societies face many social parasites that exploit their altruistic behaviours or their resources. Due to the fitness costs these social parasites incur, hosts have evolved various behavioural, chemical, architectural and morphological defence traits. Similar to bacteria infecting multicellular hosts, social parasites have to successfully go through several steps to exploit their hosts. Here, we review how social insects try to interrupt this sequence of events. They can avoid parasite contact by choosing to nest in parasite-free locales or evade attacks by adapting their colony structure. Once social parasites attack, hosts attempt to detect them, which can be facilitated by adjustme…
Temnothorax pilagens sp. n. – a new slave-making species of the tribe Formicoxenini from North America (Hymenoptera, Formicidae)
A new species of the ant genus Temnothorax Forel, 1890 – Temnothorax pilagens sp. n. is described from eastern North America. T. pilagens sp. n. is an obligate slave-making ant with two known hosts: T. longispinosus (Roger, 1863) and T. ambiguus (Emery, 1895). A differential diagnosis against Temnothorax duloticus (Wesson, 1937), the other dulotic congener from the Nearctic, is presented and a biological characteristics of the new species is given.
No inbreeding depression but increased sexual investment in highly inbred ant colonies.
Inbreeding can lead to the expression of deleterious recessive alleles and to a subsequent fitness reduction. In Hymenoptera, deleterious alleles are purged in haploid males moderating inbreeding costs. However, in these haplodiploid species, inbreeding can result in the production of sterile diploid males. We investigated the effects of inbreeding on the individual and colony level in field colonies of the highly inbred ant Hypoponera opacior. In this species, outbreeding winged sexuals and nest-mating wingless sexuals mate during two separate reproductive periods. We show that regular sib-matings lead to high levels of homozygosity and the occasional production of diploid males, which spo…
Supplmementary information II from Ant behaviour and brain gene expression of defending hosts depend on the ecological success of the intruding social parasite
Genome of Temnothorax longispinosus: methods, assembly and annotation
Fitness costs of worker specialization for ant societies
Division of labour is of fundamental importance for the success of societies, yet little is known about how individual specialization affects the fitness of the group as a whole. While specialized workers may be more efficient in the tasks they perform than generalists, they may also lack the flexibility to respond to rapid shifts in task needs. Such rigidity could impose fitness costs when societies face dynamic and unpredictable events, such as an attack by socially parasitic slavemakers. Here, we experimentally assess the colony-level fitness consequences of behavioural specialization in Temnothorax longispinosus ants that are attacked by the slavemaker ant T. americanus . We manipulate…
Life history evolution in social insects: a female perspective
Social insects are known for their unusual life histories with fecund, long-lived queens and sterile, short-lived workers. We review ultimate factors underlying variation in life history strategies in female social insects, whose social life reshapes common trade-offs, such as the one between fecundity and longevity. Interspecific life history variation is associated with colony size, mediated by changes in division of labour and extrinsic mortality. In addition to the ratio of juvenile to adult mortality, social factors such as queen number influence life history trajectories. We discuss two hypotheses explaining why queen fecundity and lifespan is higher in single-queen societies and sugg…
Ant recognition cue diversity is higher in the presence of slavemaker ants
Social insect colonies defend themselves from intruders through nestmate recognition, yet the evolution and maintenance of recognition cue diversity is still poorly understood. We compared the recognition cue diversity of 9 populations of Temnothorax longispinosus ant colonies, including populations that harbored the socially parasitic slavemaker ant, Protomognathus americanus. Although ants recognize friends from foe based on recognition cues encoded in their cuticular hydrocarbon profile, which specific compounds are involved in recognition is unknown for most species. We therefore started by statistically identifying 9 putative recognition compounds involved in worker and colony aggressi…
Forewarned is forearmed: aggression and information use determine fitness costs of slave raids
Many animals use reliable indicators of upcoming events such as antagonistic interactions to prepare themselves. In group-living animals, not only the cue perceiving individuals are involved in mobilization, but the entire group can use this information. In this study, we analyze whether social insects, which perceive reliable information on an upcoming social parasite attack, can use this knowledge to better defend their colony. We focus on the interaction between the ant Temnothorax longispinosus and the slave-making ant Protomognathus americanus, which conducts destructive raids on host colonies to steal their brood. As a behavioral defense, host colonies show aggression, which has a con…
Convergent Loss of Chemoreceptors across Independent Origins of Slave-Making in Ants
The evolution of an obligate parasitic lifestyle often leads to the reduction of morphological and physiological traits, which may be accompanied by loss of genes and functions. Slave-maker ants are social parasites that exploit the work force of closely related ant species for social behaviours such as brood care and foraging. Recent divergence between these social parasites and their hosts enables comparative studies of gene family evolution. We sequenced the genomes of eight ant species, representing three independent origins of ant slavery. During the evolution of eusociality, chemoreceptor genes multiplied due to the importance of chemical communication in societies. We investigated ev…
Supplementary information I from Ant behaviour and brain gene expression of defending hosts depend on the ecological success of the intruding social parasite
Tables and additional figures and methods details
Evidence for a conserved queen-worker genetic toolkit across slave-making ants and their ant hosts
AbstractThe ecological success of social Hymenoptera (ants, bees, wasps) depends on the division of labour between the queen and workers. Each caste is highly specialised in its respective function in morphology, behaviour and life-history traits, such as lifespan and fecundity. Despite strong defences against alien intruders, insect societies are vulnerable to social parasites, such as workerless inquilines or slave-making (dulotic) ants. Here, we investigate whether gene expression varies in parallel ways between lifestyles (slave-making versus host ants) across five independent origins of ant slavery in the “Formicoxenus-group” of the ant tribe Crematogastrini. As caste differences are o…
Comparative analyses of caste, sex, and developmental stage‐specific transcriptomes in two Temnothorax ants
Abstract Social insects dominate arthropod communities worldwide due to cooperation and division of labor in their societies. This, however, makes them vulnerable to exploitation by social parasites, such as slave‐making ants. Slave‐making ant workers pillage brood from neighboring nests of related host ant species. After emergence, host workers take over all nonreproductive colony tasks, whereas slavemakers have lost the ability to care for themselves and their offspring. Here, we compared transcriptomes of different developmental stages (larvae, pupae, and adults), castes (queens and workers), and sexes of two related ant species, the slavemaker Temnothorax americanus and its host Temnoth…
The parasite's long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host.
Parasites can induce alterations in host phenotypes in order to enhance their own survival and transmission. Parasites of social insects might not only benefit from altering their individual hosts, but also from inducing changes in uninfected group members. Temnothorax nylanderi ant workers infected with the tapeworm Anomotaenia brevis are known to be chemically distinct from nest-mates and do not contribute to colony fitness, but are tolerated in their colonies and well cared for. Here, we investigated how tapeworm- infected workers affect colony aggression by manipulating their presence in ant colonies and analysing whether their absence or presence resulted in behavioural alterations in…
The ecological success of a social parasite increases with manipulation of collective host behaviour.
Many parasites alter the behaviour of their host to their own advantage, yet hosts often vary in their susceptibility to manipulation. The ecological and evolutionary implications of such variation can be profound, as resistant host populations may suffer lower parasite pressures than those susceptible to manipulation. To test this prediction, we assessed parasite-induced aggressive behaviours across 16 populations of two Temnothorax ant species, many of which harbour the slavemaker ant Protomognathus americanus. This social parasite uses its Dufour's gland secretions to manipulate its hosts into attacking nestmates, which may deter defenders away from itself during invasion. We indeed find…
Social isolation causes downregulation of immune and stress response genes and behavioural changes in a social insect
Humans and other social mammals experience isolation from their group as stressful, triggering behavioural and physiological anomalies that reduce fitness. While social isolation has been intensely studied in social mammals, it is less clear how social insects, which evolved sociality independently, respond to isolation. Here we examined whether the typical mammalian responses to social isolation, e.g., an impaired ability to interact socially and immune suppression are also found in social insects. We studied the consequences of social isolation on behaviour and brain gene expression in the ant Temnothorax nylanderi. Following isolation, workers interacted moderately less with adult nestma…
Collective defence portfolios of ant hosts shift with social parasite pressure
Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host's nest defence, host colonies should resor…
Geographic Variation in Social Parasite Pressure Predicts Intraspecific but not Interspecific Aggressive Responses in Hosts of a Slavemaking Ant
Variation in community composition over a species' geographic range leads to divergent selection pressures, resulting in interpopulation variation in trait expression. One of the most pervasive selective forces stems from antagonists such as parasites. Whereas hosts of microparasites developed sophisticated immune systems, social parasites select for behavioural host defences. Here, we investigated the link between parasite pressure exerted by the socially parasitic slavemaking ant Protomognathus americanus and colony-level aggression in Temnothorax ants from 17 populations. We studied almost the entire geographic range of two host species, including unparasitized populations. As previous s…
Ant behaviour and brain gene expression of defending hosts depend on the ecological success of the intruding social parasite.
The geographical mosaic theory of coevolution predicts that species interactions vary between locales. Depending on who leads the coevolutionary arms race, the effectivity of parasite attack or host defence strategies will explain parasite prevalence. Here, we compare behaviour and brain transcriptomes of Temnothorax longispinosus ant workers when defending their nest against an invading social parasite, the slavemaking ant Temnothorax americanus . A full-factorial design allowed us to test whether behaviour and gene expression are linked to parasite pressure on host populations or to the ecological success of parasite populations. Albeit host defences had been shown before to covary with …
Excel table with differentially expressed genes slavemaker origin from Ant behaviour and brain gene expression of defending hosts depend on the ecological success of the intruding social parasite
slavemaker origin
Data from: No inbreeding depression but increased sexual investment in highly inbred ant colonies
Inbreeding can lead to the expression of deleterious recessive alleles and to a subsequent fitness reduction. In Hymenoptera, deleterious alleles are purged in haploid males moderating inbreeding costs. However, in these haplo-diploid species, inbreeding can result in the production of sterile diploid males. We investigated the effects of inbreeding on the individual and colony level in field colonies of the highly inbred ant Hypoponera opacior. In this species, outbreeding winged sexuals and nest-mating wingless sexuals mate during two separate reproductive periods. We show that regular sib-matings lead to high levels of homozygosity and the occasional production of diploid males, which sp…
Excel Table with differentially expressed genes host origin from Ant behaviour and brain gene expression of defending hosts depend on the ecological success of the intruding social parasite
Host origin
Data from: The parasite’s long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host
Parasites can induce alterations in host phenotypes in order to enhance their own survival and transmission. Parasites of social insects might not only benefit from altering their individual hosts, but also from inducing changes in uninfected group members. Temnothorax nylanderi ant workers infected with the tapeworm Anomotaenia brevis are known to be chemically distinct from nestmates and do not contribute to colony fitness, but are tolerated in their colonies and well cared-for. Here, we investigated how infected workers affect colony aggression by manipulating the presence of tapeworm-infected workers and analysing whether their absence or presence resulted in behavioural alterations in …
Data from: Fitness costs of worker specialisation for ant societies
Division of labour is of fundamental importance for the success of societies, yet little is known about how individual specialization affects the fitness of the group as a whole. While specialized workers may be more efficient in the tasks they perform than generalists, they may also lack the flexibility to respond to rapid shifts in task needs. Such rigidity could impose fitness costs when societies face dynamic and unpredictable events, such as an attack by socially parasitic slavemakers. Here, we experimentally assess the colony-level fitness consequences of behavioural specialization in Temnothorax longispinosus ants that are attacked by the slavemaker ant T. americanus. We manipulated …
Data from: Collective defence portfolios of ant hosts shift with social parasite pressure
Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host's nest defence, host colonies should resort…
Excel Table with differentially expressed genes parasite success and attack from Ant behaviour and brain gene expression of defending hosts depend on the ecological success of the intruding social parasite
Parasite success and attack no Attack