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.

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.

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'.

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.

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.

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.

Rugitermesursulae (Isoptera, Kalotermitidae), a new drywood termite from the Caribbean coast of Colombia.

Rugitermesursulae sp. nov. is described from a sample collected inside a dead branch in a tropical dry forest of Colombia's Caribbean coast using molecular information and external morphological characters of the imago and soldier castes. Rugitermesursulae sp. nov. soldiers and imagoes are the smallest among all described Rugitermes species. The imago's head capsule coloration is dark castaneous, while the pronotum is contrastingly pale yellow. Our description includes soldier characters, such as subflangular elevation and shape of the antennal sockets, that can help in identification of samples lacking imagoes.

Molecular underpinnings of division of labour among workers in a socially complex termite.

Division of labour characterizes all major evolutionary transitions, such as the evolution of eukaryotic cells or multicellular organisms. Social insects are characterized by reproductive division of labour, with one or a few reproducing individuals (queens) and many non-reproducing nestmates (workers) forming a colony. Among the workers, further division of labour can occur with different individuals performing different tasks such as foraging, brood care or building. While mechanisms underlying task division are intensively studied in social Hymenoptera, less is known for termites, which independently evolved eusociality. We investigated molecular mechanisms underlying task division in termite workers to test for communality with social Hymenoptera. We compared similar-aged foraging workers with builders of the fungus-growing termite Macrotermes bellicosus using transcriptomes, endocrine measures and estimators of physiological condition. Based on results for social Hymenoptera and theory, we tested the hypotheses that (i) foragers are in worse physiological conditions than builders, (ii) builders are more similar in their gene expression profile to queens than foragers are, and (iii) builders invest more in anti-ageing mechanism than foragers. Our results support all three hypotheses. We found storage proteins to underlie task division of these similar-aged termite workers and these genes also characterize reproductive division of labour between queens and workers. This implies a co-option of nutrient-based pathways to regulate division of labour across lineages of termites and social Hymenoptera, which are separated by more than 133 million years.

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.

Transcriptomic analyses of the termite, Cryptotermes secundus, reveal a gene network underlying a long lifespan and high fecundity.

Organisms are typically characterized by a trade-off between fecundity and longevity. Notable exceptions are social insects. In insect colonies, the reproducing caste (queens) outlive their non-reproducing nestmate workers by orders of magnitude and realize fecundities and lifespans unparalleled among insects. How this is achieved is not understood. Here, we identified a single module of co-expressed genes that characterized queens in the termite species Cryptotermes secundus. It encompassed genes from all essential pathways known to be involved in life-history regulation in solitary model organisms. By manipulating its endocrine component, we tested the recent hypothesis that re-wiring along the nutrient-sensing/endocrine/fecundity axis can account for the reversal of the fecundity/longevity trade-off in social insect queens. Our data from termites do not support this hypothesis. However, they revealed striking links to social communication that offer new avenues to understand the re-modelling of the fecundity/longevity trade-off in social insects.

The effect of environmental stress on ageing in a termite species with low social complexity.

Social insects seem to have overcome the almost universal trade-off between fecundity and longevity as queens can be highly fecund and at the same time reach lifespans of decades. By contrast, their non-reproducing workers are often short-lived. One hypothesis to explain the long lifespan of queens is that they are better protected against stress than their workers. However, evidence is controversial and experimental studies are scarce. We aimed at manipulating environmental stress and ageing by exposing colonies of the less-socially complex termite Cryptotermes secundus to temperature regimes that differed in variance. In contrast with expectation, constant temperatures imposed more stress than variable temperatures. Survival of queens and workers as well as queens' fecundity were partly reduced under constant conditions and both castes showed signs of ageing in the transcriptome signature under constant conditions. There was a clear oxidative stress defence signal under constant conditions that was, surprisingly, stronger for workers than queens. We discuss how our results relate to social complexity. We argue that workers that are totipotent to become reproductives, like in C. secundus, should invest more in 'anti-ageing' mechanisms than sterile workers because the former can still reproduce and have not reached maturity yet. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects.

The exceptional longevity of social insect queens despite their lifelong high fecundity remains poorly understood in ageing biology. To gain insights into the mechanisms that might underlie ageing in social insects, we compared gene expression patterns between young and old castes (both queens and workers) across different lineages of social insects (two termite, two bee and two ant species). After global analyses, we paid particular attention to genes of the insulin/insulin-like growth factor 1 signalling (IIS)/target of rapamycin (TOR)/juvenile hormone (JH) network, which is well known to regulate lifespan and the trade-off between reproduction and somatic maintenance in solitary insects. Our results reveal a major role of the downstream components and target genes of this network (e.g. JH signalling, vitellogenins, major royal jelly proteins and immune genes) in affecting ageing and the caste-specific physiology of social insects, but an apparently lesser role of the upstream IIS/TOR signalling components. Together with a growing appreciation of the importance of such downstream targets, this leads us to propose the TI-J-LiFe (TOR/IIS-JH-Lifespan and Fecundity) network as a conceptual framework for understanding the mechanisms of ageing and fecundity in social insects and beyond. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

Ageing and sociality: why, when and how does sociality change ageing patterns?

Individual lifespans vary tremendously between and also within species, but the proximate and ultimate causes of different ageing speeds are still not well understood. Sociality appears to be associated with the evolution of greater longevity and probably also with a larger plasticity of the shape and pace of ageing. For example, reproductives of several termites and ants reach lifespans that surpass those of their non-reproductive nestmates by one or two decades. In this issue, 15 papers explore the interrelations between sociality and individual longevity in both, group-living vertebrates and social insects. Here, we briefly give an overview of the contents of the various contributions, including theoretical and comparative studies, and we explore the similarities and dissimilarities in proximate mechanisms underlying ageing among taxa, with particular emphasis on nutrient-sensing pathways and, in insects, juvenile hormone. These studies point to an underestimated role of more downstream processes. We highlight the need for reliable transcriptomic markers of ageing and a comprehensive ageing theory of social animals, which includes the reproductive potential of workers, and considers the fact that social insect queens reach maturity only after a prolonged period of producing non-reproductive workers. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

Oxidative stress and senescence in social insects: a significant but inconsistent link?

The life-prolonging effects of antioxidants have long entered popular culture, but the scientific community still debates whether free radicals and the resulting oxidative stress negatively affect longevity. Social insects are intriguing models for analysing the relationship between oxidative stress and senescence because life histories differ vastly between long-lived reproductives and the genetically similar but short-lived workers. Here, we present the results of an experiment on the accumulation of oxidative damage to proteins, and a comparative analysis of the expression of 20 selected genes commonly involved in managing oxidative damage, across four species of social insects: a termite, two bees and an ant. Although the source of analysed tissue varied across the four species, our results suggest that oxidative stress is a significant factor in senescence and that its manifestation and antioxidant defenses differ among species, making it difficult to find general patterns. More detailed and controlled investigations on why responses to oxidative stress may differ across social species may lead to a better understanding of the relations between oxidative stress, antioxidants, social life history and senescence. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

A comparison of termite assemblages from West African savannah and forest ecosystems using morphological and molecular markers.

Termites (Isoptera) are important ecosystem engineers of tropical ecosystems. However, they are notoriously difficult to identify, which hinders ecological research. To overcome these problems, we comparatively studied termite assemblages in the two major West African ecosystems, savannah and forest, both under natural settings and along disturbance gradients. We identified all species using morphological as well as molecular markers. We hypothesized species richness to be higher in the forest than the savannah and that it declines with disturbance in both ecosystems. Overall we found more species in the forest than in the savannah. However, alpha diversity per site did not differ between both ecosystems with on average around ten species. For both ecosystems, species diversity did not decrease along the studied disturbance gradient but encounter rates did. For the forest, we did not detect a decline in soil feeding termites and an increase of fungus grower Macrotermitinae with disturbance as some other studies did. Yet, soil feeders were generally rare. Strikingly, the set of morphologically difficult-to-identify Macrotermitinae (Microtermes and Ancistrotermes) was as high in the forest as in the savannah with little species overlap between both ecosystems. Using phylogenetic community analyses, we found little evidence for strong structuring mechanisms such as environmental filtering or interspecific competition. Most local assemblages did not differ significantly from random assemblages of the regional species pool. Our study is the most comprehensive of its kind. It provides the most reliable termite species list for West Africa that builds the basis for further ecological studies.

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.

Phylogenetic Community Structure and Niche Differentiation in Termites of the Tropical Dry Forests of Colombia.

The mechanisms that structure species communities are still debated. We addressed this question for termite assemblages from tropical dry forests in Colombia. These forests are endangered and poorly understood ecosystems and termites are important ecosystem engineers in the tropics. Using biodiversity and environmental data, combined with phylogenetic community analyses, trait mapping, and stable isotopes studies, we investigated the termite community composition of three protected dry forests in Colombia. Our data suggest that the structuring mechanisms differed between sites. Phylogenetic overdispersion of termite assemblages correlated with decreasing rainfall and elevation and increasing temperature. Food niche traits-classified as feeding groups and quantified by δ15N‰ and δ13C‰ isotope signatures-were phylogenetically conserved. Hence, the overdispersion pattern implies increasing interspecific competition with decreasing drier and warmer conditions, which is also supported by fewer species occurring at the driest site. Our results are in line with a hypothesis that decreased biomass production limits resource availability for termites, which leads to competition. Along with this comes a diet shift: termites from drier plots had higher δ13C signatures, reflecting higher δ13C values in the litter and more C4 plants. Our study shows how a phylogenetic community approach combined with trait analyses can contribute to gaining the first insights into mechanisms structuring whole termite assemblages.

Long live the queen, the king and the commoner? Transcript expression differences between old and young in the termite Cryptotermes secundus.

Social insects provide promising new avenues for aging research. Within a colony, individuals that share the same genetic background can differ in lifespan by up to two orders of magnitude. Reproducing queens (and in termites also kings) can live for more than 20 years, extraordinary lifespans for insects. We studied aging in a termite species, Cryptotermes secundus, which lives in less socially complex societies with a few hundred colony members. Reproductives develop from workers which are totipotent immatures. Comparing transcriptomes of young and old individuals, we found evidence for aging in reproductives that was especially associated with DNA and protein damage and the activity of transposable elements. By contrast, workers seemed to be better protected against aging. Thus our results differed from those obtained for social insects that live in more complex societies. Yet, they are in agreement with lifespan estimates for the study species. Our data are also in line with expectations from evolutionary theory. For individuals that are able to reproduce, it predicts that aging should only start after reaching maturity. As C. secundus workers are immatures with full reproductive options we expect them to invest into anti-aging processes. Our study illustrates that the degree of aging can differ between social insects and that it may be associated with caste-specific opportunities for reproduction.

Termite Communities along A Disturbance Gradient in a West African Savanna.

(1) Background: Termites are important ecosystem engineers, crucial for the maintenance of tropical biodiversity and ecosystem functioning. But they are also pests which cause billions of dollars in damage annually to humans. Currently, our understanding of the mechanisms influencing species occurrences is limited and we do not know what distinguishes pest from non-pest species. (2) Method: We analyzed how anthropogenic disturbance (agriculture) affects species occurrences. We tested the hypothesis that strong disturbance functions as a habitat filter and selects for a subset of species which are major pests of crop. Using a cross-sectional approach, we studied termite assemblage composition along a disturbance gradient from fields to 12-year-old fallows in a West African savanna. (3) Results: We reliably identified 19 species using genetic markers with a mean of about 10 species-many of them from the same feeding type-co-occurring locally. Supporting our hypothesis, disturbance was associated with environmental filtering of termites from the regional species pool, maybe via its effect on vegetation type. The most heavily disturbed sites were characterized by a subset of termite species which are well-known pests of crop. (4) Conclusion: These results are in line with the idea that strong anthropogenic disturbance selects for termite pest species.

Termite Taxonomy, Challenges and Prospects: West Africa, A Case Example.

Termites are important ecosystem engineers. Yet they are often difficult to identify due to the lack of reliable species-specific morphological traits for many species, which hampers ecological research. Recently, termitologists working with West African termites (West African Termite Taxonomy Initiative) convened for a workshop with the aim of beginning to address this problem. Repeated determination of the same termite samples by the most renowned taxonomists for West African termites identified the huge scale of the problem, as less than 10% of all species could be unambiguously determined to the species level. Intensive discussions and comparisons increased the identification success to around 25% at the end of the workshop. Yet many groups remained problematic and molecular markers and barcoding techniques combined with species delimitation approaches will be needed to help resolve these existing taxonomic problems. Based on the outcome of this workshop, we propose concerted initiatives to address termite taxonomy on a global scale. We are convinced that dedicated workshops on regional taxonomy that follow a similar structured approach, with repeated determination of the same sample, will help overcome the difficulties that termite taxonomy faces. This initiative can also serve as a blueprint for other taxonomical groups that are difficult to identify.