Mating system and population genetic structure of the bulldog ant Myrmecia pavida

Understanding the evolution of the alternative mating strategies of monandry and polyandry is a fundamental problem in evolutionary biology because of the cost-benefit trade-offs associated with mating for females. The problem is particularly intriguing in the social insects because queens in most species appear to be obligately monandrous (i.e., only a single male fathers their offspring), while those in a minority of species have evolved high, and sometimes extreme, polyandry. One group which may shed particular insight is the ant subfamily Myrmeciinae (Myrmecia and Nothomyrmecia). Here we examine the population and colony genetic structure of the bulldog ant Myrmecia pavida CLARK, 1951 by genotyping offspring workers from 45 colonies. We find little evidence of geographic structuring or inbreeding in the population, indicating that the species outbreeds, most probably in mating swarms. We also find that queens of M pavida show moderately high polyandry, with 84% having mated with between two and seven males, and an overall mean observed mating frequency of 3.8. This is significantly higher than previously reported for queens of Nothomyrmecia macrops, in which most females mate singly. This was similar to that of M pyriformis, M brevinoda, and M pilosula, the three congenerics for which mating frequencies have recently been reported. The two genera in the Myrmeciinae therefore appear to show multiple transitions in mating frequency and further investigation of the subfamily may be highly informative for disentangling the forces driving the evolution of alternative mating strategies

Division of labour and risk taking in the dinosaur ant, Dinoponera quadriceps

The success of social insects can be largely attributed to division of labour. In contrast to most social insects, many species with simple societies contain workers which are capable of sexual reproduction. Headed by one or a few reproductive individuals, subordinate workers form a dominance hierarchy, queuing to attain the reproductive role. In these species task allocation may be influenced by individual choice based on future reproductive prospects. Individuals with a better chance of inheriting the colony may be less likely to take risks and high-ranking workers that spend a greater amount of time in proximity to the brood may be able to increase the ability to police egg-laying by cheating subordinates. We investigated division of labour and risk taking in relation to dominance rank in the queenless ponerine ant, Dinoponera quadriceps, a species with relatively simple societies. Using behavioural observations, we show that high-ranking workers spend more time performing egg care, less time foraging and are less likely to defend the nest against attack. High-rankers also spent a greater amount of time guarding and inspecting eggs, behaviours which are likely to improve detection of egg laying by cheating subordinates. We also show that high-ranking workers spend a greater amount of time idle, which may help increase lifespan by reducing energy expenditure. Our results suggest that both risk-taking and egg-care behaviours are related to future reproductive prospects in D. quadriceps. This highlights a mechanism by which effective division of labour could have been achieved during the early stages of eusocial evolution

Behavioural effects of juvenile hormone and their influence on division of labour in leaf-cutting ant societies

Division of labour in social insects represents a major evolutionary transition, but the physiological mechanisms that regulate this are still little understood. Experimental work with honey bees, and correlational analyses in other social insects, have implicated juvenile hormone (JH) as a regulatory factor, but direct experimental evidence of behavioural effects of JH in social insects is generally lacking. Here, we used experimental manipulation of JH to show that raised JH levels in leaf-cutting ants results in workers becoming more active, phototactic and threat responsive, and engaging in more extranidal activity – behavioural changes that we show are all characteristic of the transition from intranidal work to foraging. These behavioural effects on division of labour suggest that the JH mediation of behaviour occurs across multiple independent evolutions of eusociality, and may be a key endocrine regulator of the division of labour which has produced the remarkable ecological and evolutionary success of social insects

Short-term heat stress results in diminution of bacterial symbionts but has little effect on life history in adult female citrus mealybugs

Mealybugs are sap-feeding insect pests that pose a serious threat to horticulture. The citrus mealybug, Planococcus citri (Risso) (Hemiptera: Pseudococcidae), like most other mealybug species, harbours two obligate maternally transmitted bacterial endosymbionts, which are essential for nutrient acquisition and host survival. These are ‘Candidatus Tremblaya princeps’, a member of the β-Proteobacteria, and ‘Candidatus Moranella endobia’, a member of the γ-Proteobacteria. The density of symbionts in the hosts is now understood to be dynamic, being influenced by the age and gender of the host and by environmental conditions during development. Here, we examine the impact of short-term heat stress treatment on the obligate symbionts and life-history parameters of P. citri, using qPCR to measure changes in symbiont density. Heat stress killed juveniles and adult males, and significantly reduced levels of ‘Ca. Moranella endobia’ and ‘Ca. Tremblaya princeps’ in adult females. However, adult females were resilient to this and it did not affect their fecundity or brood survival, although the sex ratio of their brood was slightly, but significantly, more female biased. Our results suggest that ‘Ca. Tremblaya princeps’ and ‘Ca. Moranella endobia’ are not as essential to the survival of adult mealybugs as they are to the survival of immature mealybugs and that sub-lethal heat treatment alone is unlikely to be effective as a disinfestation tactic

Quality and quantity: transitions in antimicrobial gland use for parasite defense

Parasites are a major force in evolution, and understanding how host life history affects parasite pressure and investment in disease resistance is a general problem in evolutionary biology. The threat of disease may be especially strong in social animals, and ants have evolved the unique metapleural gland (MG), which in many taxa produce antimicrobial compounds that have been argued to have been a key to their ecological success. However, the importance of the MG in the disease resistance of individual ants across ant taxa has not been examined directly. We investigate experimentally the importance of the MG for disease resistance in the fungus-growing ants, a group in which there is interspecific variation in MG size and which has distinct transitions in life history. We find that more derived taxa rely more on the MG for disease resistance than more basal taxa and that there are a series of evolutionary transitions in the quality, quantity, and usage of the MG secretions, which correlate with transitions in life history. These shifts show how even small clades can exhibit substantial transitions in disease resistance investment, demonstrating that host–parasite relationships can be very dynamic and that targeted experimental, as well as large-scale, comparative studies can be valuable for identifying evolutionary transitions

A mechanistic framework to explain the immunosuppressive effects of neurotoxic pesticides on bees

1. There is growing concern that declines in some managed and wild bee pollinator populations threaten biodiversity, the functioning of vital ecological processes and sustainable food production on a global scale. 2. In recent years, there has been increasing evidence that sub-lethal exposure to the neurotoxic class of insecticides (neonicotinoids) can undermine pollinator immunocompetence and amplify the effects of diseases, which have been suspected to be one of the drivers of pollinator declines. However, exactly how neonicotinoids might inhibit pollinator immunity remains elusive. 3. Here we put forward a mechanistic framework to explain the effects of neurotoxic pesticides on insect immunocompetence. We propose that there is a close ontogenetic connection between the cellular arm (haemocytes) of the insect immune and nervous systems, and that this connection makes the immune system of pollinators and other insects inherently susceptible to interference by neurotoxins such as neonicotinoids at sublethal doses. 4. Investigation of this connection is urgently needed to confirm the validity of this framework, and develop a clear, mechanistically-informed understanding of the interplay between neonicotinoids and disease ecology in pollinators. This in turn may enable us to develop strategies to mitigate impacts of neurotoxins on pollinators and/or enhance their impacts on pests

Sperm mixing in the polyandrous leaf-cutting ant Acromyrmex echinatior

The insemination of queens by sperm from multiple males (polyandry) has evolved in a number of eusocial insect lineages despite the likely costs of the behavior. The selective advantages in terms of colony fitness must therefore also be significant and there is now good evidence that polyandry increases genetic variation among workers, thereby improving the efficiency of division of labor, resistance against disease, and diluting the impact of genetically incompatible matings. However, these advantages will only be maximized if the sperm of initially discrete ejaculates are mixed when stored in queen spermathecae and used for egg fertilization in a “fair raffle.” Remarkably, however, very few studies have addressed the level of sperm mixing in social insects. Here we analyzed sperm use over time in the highly polyandrous leaf-cutting ant Acromyrmex echinatior. We genotyped cohorts of workers produced either 2 months apart or up to over a year apart, and batches of eggs laid up to over 2 years apart, and tested whether fluctuations in patriline distributions deviated from random. We show that the representation of father males in both egg and worker cohorts does not change over time, consistent with obligatorily polyandrous queens maximizing their fitness when workers are as genetically diverse as possible

Disease management in two sympatric Apterostigma fungus-growing ants for controlling the parasitic fungus Escovopsis

Antagonistic interactions between host and parasites are often embedded in networks of interacting species, in which hosts may be attacked by competing parasites species, and parasites may infect more than one host species. To better understand the evolution of host defenses and parasite counterdefenses in the context of a multihost, multiparasite system, we studied two sympatric species, of congeneric fungus-growing ants (Attini) species and their symbiotic fungal cultivars, which are attacked by multiple morphotypes of parasitic fungi in the genus, Escovopsis. To assess whether closely related ant species and their cultured fungi are evolving defenses against the same or different parasitic strains, we characterized Escovopsis that were isolated from colonies of sympatric Apterostigma dentigerum and A. pilosum. We assessed in vitro and in vivo interactions of these parasites with their hosts. While the ant cultivars are parasitized by similar Escovopsis spp., the frequency of infection by these pathogens differs between the two ant species. The ability of the host fungi to suppress Escovopsis growth, as well as ant defensive responses toward the parasites, differs depending on the parasite strain and on the host ant species