The remoulding of dietary effects on the fecundity / longevity trade-off in a social insect.

BACKGROUND: In many organisms increased reproductive effort is associated with a shortened life span. This trade-off is reflected in conserved molecular pathways that link nutrient-sensing with fecundity and longevity. Social insect queens apparently defy the fecundity / longevity trade-off as they are both, extremely long-lived and highly fecund. Here, we have examined the effects of a protein-enriched diet on these life-history traits and on tissue-specific gene expression in a termite species of low social complexity. RESULTS: On a colony level, we did not observe reduced lifespan and increased fecundity, effects typically seen in solitary model organisms, after protein enrichment. Instead, on the individual level mortality was reduced in queens that consumed more of the protein-enriched diet - and partially also in workers - while fecundity seemed unaffected. Our transcriptome analyses supported our life-history results. Consistent with life span extension, the expression of IIS (insulin/insulin-like growth factor 1 signalling) components was reduced in fat bodies after protein enrichment. Interestingly, however, genes involved in reproductive physiology (e.g., vitellogenin) were largely unaffected in fat body and head transcriptomes. CONCLUSION: These results suggest that IIS is decoupled from downstream fecundity-associated pathways, which can contribute to the remoulding of the fecundity/longevity trade-off in termites as compared to solitary insects.

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.

Disentangling the aging gene expression network of termite queens.

BACKGROUND: Most insects are relatively short-lived, with a maximum lifespan of a few weeks, like the aging model organism, the fruit-fly Drosophila melanogaster. By contrast, the queens of many social insects (termites, ants and some bees) can live from a few years to decades. This makes social insects promising models in aging research providing insights into how a long reproductive life can be achieved. Yet, aging studies on social insect reproductives are hampered by a lack of quantitative data on age-dependent survival and time series analyses that cover the whole lifespan of such long-lived individuals. We studied aging in queens of the drywood termite Cryptotermes secundus by determining survival probabilities over a period of 15 years and performed transcriptome analyses for queens of known age that covered their whole lifespan. RESULTS: The maximum lifespan of C. secundus queens was 13 years, with a median maximum longevity of 11.0 years. Time course and co-expression network analyses of gene expression patterns over time indicated a non-gradual aging pattern. It was characterized by networks of genes that became differentially expressed only late in life, namely after ten years, which associates well with the median maximum lifespan for queens. These old-age gene networks reflect processes of physiological upheaval. We detected strong signs of stress, decline, defense and repair at the transcriptional level of epigenetic control as well as at the post-transcriptional level with changes in transposable element activity and the proteostasis network. The latter depicts an upregulation of protein degradation, together with protein synthesis and protein folding, processes which are often down-regulated in old animals. The simultaneous upregulation of protein synthesis and autophagy is indicative of a stress-response mediated by the transcription factor cnc, a homolog of human nrf genes. CONCLUSIONS: Our results show non-linear senescence with a rather sudden physiological upheaval at old-age. Most importantly, they point to a re-wiring in the proteostasis network and stress as part of the aging process of social insect queens, shortly before queens die.

Longevity and transposon defense, the case of termite reproductives.

Social insects are promising new models in aging research. Within single colonies, longevity differences of several magnitudes exist that can be found elsewhere only between different species. Reproducing queens (and, in termites, also kings) can live for several decades, whereas sterile workers often have a lifespan of a few weeks only. We studied aging in the wild in a highly social insect, the termite Macrotermes bellicosus, which has one of the most pronounced longevity differences between reproductives and workers. We show that gene-expression patterns differed little between young and old reproductives, implying negligible aging. By contrast, old major workers had many genes up-regulated that are related to transposable elements (TEs), which can cause aging. Strikingly, genes from the PIWI-interacting RNA (piRNA) pathway, which are generally known to silence TEs in the germline of multicellular animals, were down-regulated only in old major workers but not in reproductives. Continued up-regulation of the piRNA defense commonly found in the germline of animals can explain the long life of termite reproductives, implying somatic cooption of germline defense during social evolution. This presents a striking germline/soma analogy as envisioned by the superorganism concept: the reproductives and workers of a colony reflect the germline and soma of multicellular animals, respectively. Our results provide support for the disposable soma theory of aging.

Correlates of blood parasitism in a threatened marshland passerine: infection by kinetoplastids of the genus Trypanosoma is related to landscape metrics of habitat edge.

In birds, vector-borne parasites invading the bloodstream are important agents of disease, affect fitness and shape population viability, thus being of conservation interest. Here, we molecularly identified protozoan blood parasites in two populations of the threatened Aquatic Warbler Acrocephalus paludicola, a migratory passerine nesting in open marsh. We explored whether prevalence and lineage diversity of the parasites vary by population and whether infection status is explained by landscape metrics of habitat edge and individual traits (body mass, fat score, wing length and sex). Aquatic Warblers were infected by genera Plasmodium, Leucocytozoon and Trypanosoma, with seven, one and four lineages, and 29.9, 0.7 and 12.5% prevalence, respectively. No Haemoproteus infections were detected. Prevalence did not vary between the populations, but lineage diversity was higher in Polesie than in Biebrza for all the lineages pooled and for Plasmodium. Infection by Trypanosoma decreased with patch core area and increased with density of habitat edge. Infection status was not predicted by the individual traits. Our study is the first to show an association between edge-related landscape features and blood parasitism in an open habitat bird. This finding will support informed conservation measures for avian species of the globally shrinking marshland and other treeless habitats.

Reconstructed evolution of insulin receptors in insects reveals duplications in early insects and cockroaches.

Social insects show an extreme degree of phenotypic plasticity. In highly eusocial species, this manifests in the generation of distinct castes with extreme differences in both morphology and life span. The molecular basis of these differences is highly entangled and not fully understood, but several recent studies demonstrated that insulin/insulin-like growth factor signaling (IIS) is one of the key pathways. Here, we investigate the molecular evolution of insect insulin receptors (InRs), which are membrane-bound dimers that enable IIS by relaying extracellular signals to intracellular signaling cascades. Classic models of invertebrate IIS include only one InR gene, but some recent studies on less commonly studied insects have found two InRs, which act in an antagonistic manner to facilitate polyphenism in at least one documented case. We search 22 arthropod genomes and identify several InR copies and their evolutionary origin that were lacking from previous annotations. Phylogenetic analysis shows that the two insect InR genes date back at least 400 million years to a common ancestor of winged insects. Most notably, we also identified the evolutionary origin of a third InR copy that is unique to the clade of Blattodea, just before therein the eusocial termites evolved. One of the InR paralogs consistently shows caste-biased expression in all three termites, which strongly suggests a role in caste differentiation. These results have important ramifications for past and future InR inhibition/InR knockdown experiments in insects and they provide a set of key genes regulating life span and morphology in termite castes.

Remodeling of the juvenile hormone pathway through caste-biased gene expression and positive selection along a gradient of termite eusociality.

The evolution of division of labor between sterile and fertile individuals represents one of the major transitions in biological complexity. A fascinating gradient in eusociality evolved among the ancient hemimetabolous insects, ranging from noneusocial cockroaches through the primitively social lower termites-where workers retain the ability to reproduce-to the higher termites, characterized by lifetime commitment to worker sterility. Juvenile hormone (JH) is a prime candidate for the regulation of reproductive division of labor in termites, as it plays a key role in insect postembryonic development and reproduction. We compared the expression of JH pathway genes between workers and queens in two lower termites (Zootermopsis nevadensis and Cryptotermes secundus) and a higher termite (Macrotermes natalensis) to that of analogous nymphs and adult females of the noneusocial cockroach Blattella germanica. JH biosynthesis and metabolism genes ranged from reproductive female-biased expression in the cockroach to predominantly worker-biased expression in the lower termites. Remarkably, the expression profile of JH pathway genes sets the higher termite apart from the two lower termites, as well as the cockroach, indicating that JH signaling has undergone major changes in this eusocial termite. These changes go beyond mere shifts in gene expression between the different castes, as we find evidence for positive selection in several termite JH pathway genes. Thus, remodeling of the JH pathway may have played a major role in termite social evolution, representing a striking case of convergent molecular evolution between the termites and the distantly related social hymenoptera.

Chemical Fertility Signaling in Termites: Idiosyncrasies and Commonalities in Comparison with Ants.

Termites evolved eusociality independently from social Hymenoptera. As a common trait, reproductive monopoly is maintained through chemical communication. The queen (and in termites also a king) prevents workers from reproduction by conveying their reproductive status. In termites all soldiers are sterile, but workers' potential to reproduce differs between species. It ranges from totipotency in wood-dwelling lower termites where workers are a transient stage from which all other castes develop, to sterile workers in some higher termites. Intermediate are species in which workers can develop into replacement sexuals within the nest but not into winged sexuals. I summarize the patchy picture about fertility signaling that we currently have for termites, pointing also to potential conflicts over reproduction that differ from those in social Hymenoptera. Recent findings imply that, similar to many social Hymenoptera, wood-dwelling termites that live in confined nests use long-chain cuticular hydrocarbons (CHCs) as fertility signals. Yet other compounds are important as well, comprising proteinaceous secretions and especially volatiles. For a subterranean termite, two volatiles have been identified as primer pheromones that prevent reproductive differentiation of workers. It requires more data to test whether wood-dwelling termites use CHCs, while species with larger colonies and less confined nests use volatiles, or whether all species rely on multicomponent signals. Ultimately, we need more effort to model and test potential conflicts over reproduction between queens, kings and workers. Here results from social Hymenoptera cannot be transferred to termites as the latter are diploid and commonly inbred. This review illustrates promising future research avenues.

Evolution of delayed dispersal and subsequent emergence of helping, with implications for cooperative breeding.

Cooperative breeding occurs when individuals help raise the offspring of others. It is widely accepted that help displayed by cooperative breeders emerged only after individuals' tendency to delay dispersal had become established. We use this idea as a basis for two inclusive-fitness models: one for the evolution of delayed dispersal, and a second for the subsequent emergence of helpful behavior exhibited by non-breeding individuals. We focus on a territorial species in a saturated environment, and allow territories to be inherited by non-breeding individuals who have delayed dispersal. Our first model predicts that increased survivorship and increased fecundity both provide an incentive to non-breeding individuals to delay dispersal, and stay near their natal territory for some period of time. Predictions from the first model can be well understood by ignoring complications arising from competition among relatives. Our second model shows that effects on relatives play a primary role in the advantage of helping. In addition, the second model predicts that increased survivorship and fecundity promote the emergence of help. Together, our models lead us to conclude that the emergence of cooperative-breeding systems is made easier by life-history features associated with high survivorship and fecundity. We discuss the implications of our conclusions for life-history-based hypotheses of cooperative breeding and social evolution.

Complementary symbiont contributions to plant decomposition in a fungus-farming termite.

Termites normally rely on gut symbionts to decompose organic matter but the Macrotermitinae domesticated Termitomyces fungi to produce their own food. This transition was accompanied by a shift in the composition of the gut microbiota, but the complementary roles of these bacteria in the symbiosis have remained enigmatic. We obtained high-quality annotated draft genomes of the termite Macrotermes natalensis, its Termitomyces symbiont, and gut metagenomes from workers, soldiers, and a queen. We show that members from 111 of the 128 known glycoside hydrolase families are represented in the symbiosis, that Termitomyces has the genomic capacity to handle complex carbohydrates, and that worker gut microbes primarily contribute enzymes for final digestion of oligosaccharides. This apparent division of labor is consistent with the Macrotermes gut microbes being most important during the second passage of comb material through the termite gut, after a first gut passage where the crude plant substrate is inoculated with Termitomyces asexual spores so that initial fungal growth and polysaccharide decomposition can proceed with high efficiency. Complex conversion of biomass in termite mounds thus appears to be mainly accomplished by complementary cooperation between a domesticated fungal monoculture and a specialized bacterial community. In sharp contrast, the gut microbiota of the queen had highly reduced plant decomposition potential, suggesting that mature reproductives digest fungal material provided by workers rather than plant substrate.

Major Hurdles for the Evolution of Sociality.

Why do most animals live solitarily, while complex social life is restricted to a few cooperatively breeding vertebrates and social insects? Here, we synthesize concepts and theories in social evolution and discuss its underlying ecological causes. Social evolution can be partitioned into (a) formation of stable social groups, (b) evolution of helping, and (c) transition to a new evolutionary level. Stable social groups rarely evolve due to competition over food and/or reproduction. Food competition is overcome in social insects with central-place foraging or bonanza-type food resources, whereas competition over reproduction commonly occurs because staying individuals are rarely sterile. Hence, the evolution of helping is shaped by direct and indirect fitness options and helping is only altruism if it reduces the helper's direct fitness. The helper's capability to gain direct fitness also creates within-colony conflict. This prevents transition to a new evolutionary level.

The scent of royalty: a p450 gene signals reproductive status in a social insect.

Cooperation requires communication; this applies to animals and humans alike. The main communication means differ between taxa and social insects (ants, termites, and some bees and wasps) lack the cognitive abilities of most social vertebrates. Central to the regulation of the reproductive harmony in insect societies is the production of a royalty scent which signals the fertility status of the reproducing queen to the nonreproducing workers. Here, we revealed a central genetic component underlying this hallmark of insect societies in the termite Cryptotermes secundus. Communication between queens and workers relied upon the expression of a gene, Neofem4, which belongs to the cytochrome P450 genes. We inhibited Neofem4 in queens by RNA interference. This resulted in the loss of the royalty scent in queens and the workers behaved as though the queen were absent. The queen's behavior was not generally affected by silencing Neofem4. This suggests that the lack of the royalty scent lead to workers not recognizing her anymore as queen. P450 genes are known to be involved in the production of chemical signals in cockroaches and their expression has been linked to a major fertility regulator, juvenile hormone. This makes P450 genes, both a suitable and available evolutionary substrate in the face of natural selection for production of a queen substance. Our data suggest that in an organism without elaborate cognitive abilities communication has been achieved by the exploitation of a central gene that links the fertility network with the chemical communication pathway. As termites and social Hymenoptera seem to share the same class of compounds in signaling fertility, this role of P450 genes might be more widespread across social insects.

A phylogenetic community approach for studying termite communities in a West African savannah.

Termites play fundamental roles in tropical ecosystems, and mound-building species in particular are crucial in enhancing species diversity, from plants to mammals. However, it is still unclear which factors govern the occurrence and assembly of termite communities. A phylogenetic community approach and null models of species assembly were used to examine structuring processes associated with termite community assembly in a pristine savannah. Overall, we did not find evidence for a strong influence of interspecific competition or environmental filtering in structuring these communities. However, the presence of a single species, the mound-building termite Macrotermes bellicosus, left a strong signal on structuring and led to clustered communities of more closely related species. Hence, this species changes the assembly rules for a whole community. Our results show the fundamental importance of a single insect species for community processes, suggesting that more attention to insect species is warranted when developing conservation strategies.

A genetic toolkit underlying the queen phenotype in termites with totipotent workers.

Social insect castes (e.g., queens, workers) are prime examples of phenotypic plasticity (i.e., different phenotypes arising from the same genotype). Yet, the mechanisms that give rise to highly fertile, long-lived queens versus non-reproducing, short-lived workers are not well understood. Recently, a module of co-expressed genes has been identified that characterizes queens compared to workers of the termite Cryptotermes secundus (Kalotermitidae): the Queen Central Module (QCM). We tested whether the QCM is shared in termite species, in which queens gradually develop via early larval and late larval instars, the latter functioning as totipotent workers (linear development). Similar as in C. secundus, gene expression profiles revealed an enrichment of QCM genes in Zootermopsis angusticollis queens, a species from another termite family (Archotermopsidae). The expression of these QCM genes became gradually enriched during development from early larval instars via workers to queens. Thus, our results support the hypothesis of a conserved genetic toolkit that characterizes termite queens with gradual linear development. Our data also imply a strong caste-specific tissue specificity with the QCM signal being restricted to head-prothorax tissues in termite queens. This tissue-specific expression of key aging-related genes might have facilitated the evolution of a long lifespan in termite queens.

The socioecological benefits and consequences of oil palm cultivation in its native range: The Sustainable Oil Palm in West Africa (SOPWA) Project.

Agriculture is expanding rapidly across the tropics. While cultivation can boost socioeconomic conditions and food security, it also threatens native ecosystems. Oil palm (Elaeis guineensis), which is grown pantropically, is the most productive vegetable oil crop worldwide. The impacts of oil palm cultivation have been studied extensively in Southeast Asia and - to a lesser extent - in Latin America but, in comparison, very little is known about its impacts in Africa: oil palm's native range, and where cultivation is expanding rapidly. In this paper, we introduce a large-scale research programme - the Sustainable Oil Palm in West Africa (SOPWA) Project - that is evaluating the relative ecological impacts of oil palm cultivation under traditional (i.e., by local people) and industrial (i.e., by a large-scale corporation) management in Liberia. Our paper is twofold in focus. First, we use systematic mapping to appraise the literature on oil palm research in an African context, assessing the geographic and disciplinary focus of existing research. We found 757 publications occurring in 36 African countries. Studies tended to focus on the impacts of palm oil consumption on human health and wellbeing. We found no research that has evaluated the whole-ecosystem (i.e., multiple taxa and ecosystem functions) impacts of oil palm cultivation in Africa, a knowledge gap which the SOPWA Project directly addresses. Second, we describe the SOPWA Project's study design and-using canopy cover, ground vegetation cover, and soil temperature data as a case study-demonstrate its utility for assessing differences between areas of rainforest and oil palm agriculture. We outline the socioecological data collected by the SOPWA Project to date and describe the potential for future research, to encourage new collaborations and additional similar projects of its kind in West Africa. Increased research in Africa is needed urgently to understand the combined ecological and sociocultural impacts of oil palm and other agriculture in this unique region. This will help to ensure long-term sustainability of the oil palm industry-and, indeed, all tropical agricultural activity-in Africa.

Isolated in an ocean of grass: low levels of gene flow between termite subpopulations.

Habitat fragmentation is one of the most important causes of biodiversity loss, but many species are distributed in naturally patchy habitats. Such species are often organized in highly dynamic metapopulations or in patchy populations with high gene flow between subpopulations. Yet, there are also species that exist in stable patchy habitats with small subpopulations and presumably low dispersal rates. Here, we present population genetic data for the 'magnetic' termite Amitermes meridionalis, which show that short distances between subpopulations do not hinder exceptionally strong genetic differentiation (FST : 0.339; RST : 0.636). Despite the strong genetic differentiation between subpopulations, we did not find evidence for genetic impoverishment. We propose that loss of genetic diversity might be counteracted by a long colony life with low colony turnover. Indeed, we found evidence for the inheritance of colonies by so-called 'replacement reproductives'. Inhabiting a mound for several generations might result in loss of gene diversity within a colony but maintenance of gene diversity at the subpopulation level.

Epigenetic regulation and division of labor in social insects.

Analogous to multicellular organisms, social insect colonies are characterized by division of labor with queens and workers reflecting germline and soma, respectively. In multicellular organisms, such division is achieved through epigenetic factors regulating cell differentiation during development. Analogously, epigenetic regulation is postulated to regulate caste differences in social insects. We summarize recent findings about the role of epigenetics in social insects, focusing on DNA methylation and histone modifications. We specifically address (i) queen versus worker caste differentiation, (ii) queen versus worker caste differences, and (iii) division of labor among workers. Our review provides an overview of an exciting and controversially discussed field in developmental and molecular biology. It shows that our current understanding about the role of epigenetics in regulating division of labor in social insects is still fragmentary but that refined methods with well-replicated samples and targeted questions offer promising insights into this emerging field of socio-epigenomics.

Need for shared internal mound conditions by fungus-growing Macrotermes does not predict their species distributions, in current or future climates.

The large, iconic nests constructed by social species are engineered to create internal conditions buffered from external climatic extremes, to allow reproduction and/or food production. Nest-inhabiting eusocial Macrotermitinae (Blattodea: Isoptera) are outstanding palaeo-tropical ecosystem engineers that evolved fungus-growing to break down plant matter ca 62 Mya; the termites feed on the fungus and plant matter. Fungus-growing ensures a constant food supply, but the fungi need temperature-buffered, high humidity conditions, created in architecturally complex, often tall, nest-structures (mounds). Given the need for constant and similar internal nest conditions by fungi farmed by different Macrotermes species, we assessed whether current distributions of six African Macrotermes correlate with similar variables, and whether this would reflect in expected species' distribution shifts with climate change. The primary variables explaining species' distributions were not the same for the different species. Distributionally, three of the six species are predicted to see declines in highly suitable climate. For two species, range increases should be small (less than 9%), and for a single species, M. vitrialatus, 'very suitable' climate could increase by 64%. Mismatches in vegetation requirements and anthropogenic habitat transformation may preclude range expansion, however, presaging disruption to ecosystem patterns and processes that will cascade through systems at both landscape and continental scales. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Brood care and social evolution in termites.

Cooperative brood care is assumed to be the common driving factor leading to sociality. While this seems to be true for social Hymenoptera and many cooperatively breeding vertebrates, the importance of brood care for the evolution of eusociality in termites is unclear. A first step in elucidating this problem is an assessment of the ancestral condition in termites. We investigated this by determining the overall level of brood care behaviour across four termite species that cover the phylogenetic diversity of the lower termites. Brood care was low in the three species (all from different families) that had an ancestral wood-dwelling lifestyle of living in a single piece of wood that serves as food and shelter. In the fourth species, a lower termite that evolved outside foraging, brood care was more common. Together with data for higher termites, this suggests that brood care in termites only becomes important when switching from a wood-dwelling to a foraging lifestyle. These results imply that early social evolution in termites was driven by benefits of increased defence, while eusociality in Hymenoptera and cooperative breeding in birds and mammals are primarily based on brood care.

Why join a neighbour: fitness consequences of colony fusions in termites.

The evolution of life is characterized by major evolutionary transitions during which independent units cooperated and formed a new level of selection. Relatedness is a common mechanism that reduces conflict in such cooperative associations. One of the latest transitions is the evolution of social insect colonies. As expected, they are composed of kin and mechanisms have evolved that prevent the intrusion of nonrelatives. Yet, there are exceptions an extreme case is the fusion of unrelated colonies. What are the advantages of fusions that have colonies with a high potential for conflict as a consequence? Here, we investigated fitness costs and benefits of colony fusions in a lower termite species, Cryptotermes secundus, in which more than 25% of all colonies in the field are fused. We found two benefits of colony fusion depending on colony size: very small colonies had an increased probability of survival when they fused, yet for most colony sizes mainly a few workers profit from colony fusions as their chance to become reproductives increased. This individual benefit was often costly for other colony members: colony growth was reduced and the current reproductives had an increased chance of dying when fusions were aggressive. Our study suggests that fusion of colonies often is the result of 'selfish' worker interests to become reproductives, and this might have been important for the termites' social evolution. Our results uniquely shows that selfish interests among related colony members can lead to the formation of groups with increased potential for conflict among less related members.