Seirian Sumner | University College London (original) (raw)

Papers by Seirian Sumner

Biological Reviews, 2021

The aculeate wasps are one of the most diverse and speciose insect taxa; they are omnipresent acr... more The aculeate wasps are one of the most diverse and speciose insect taxa; they are omnipresent across ecosystems and exhibit diverse co-evolutionary and exploitative associations with other organisms. There is widespread conjecture that aculeate wasps are likely to perform essential ecological and economic services of importance to the health, well-being and nutritional needs of our planet. However, the scope and nature of the ecosystem services they provide are not well understood relative to other insect groups (e.g. bees, butterflies, beetles); an appreciation of their value is further tarnished by their public reputation as pointless pests. Here, we conduct the first comprehensive review of how aculeate wasps contribute to the four main areas of ecosystem services: regulatory, provisioning, supporting and cultural services. Uniting data from a large but previously disconnected literature on solitary and social aculeate wasps, we provide a synthesis on how these insects perform important ecosystem services as parasites, predators, biological indicators, pollinators, decomposers and seed dispersers; and their additional services as a sustainable alternative to meat for human consumption, and medicinal potential as sources of research leads for anti-microbials and cancer treatments. We highlight how aculeate wasps offer substantial, but largely overlooked, economic benefits through their roles in natural pest management and biological control programs. Accordingly, we provide data-driven arguments for reasons to consider the ecosystem service value of aculeate wasps on a par with other 'useful' insects (e.g. bees). Finally, we provide a research roadmap identifying the key areas of research required to capitalise better on the services provided by these important insects.

Nature, Mar 15, 2018

The evolution of altruism-costly self-sacrifice in the service of others-has puzzled biologists s... more The evolution of altruism-costly self-sacrifice in the service of others-has puzzled biologists since The Origin of Species. For half a century, attempts to understand altruism have developed around the concept that altruists may help relatives to have extra offspring in order to spread shared genes. This theory-known as inclusive fitness-is founded on a simple inequality termed Hamilton's rule. However, explanations of altruism have typically not considered the stochasticity of natural environments, which will not necessarily favour genotypes that produce the greatest average reproductive success. Moreover, empirical data across many taxa reveal associations between altruism and environmental stochasticity, a pattern not predicted by standard interpretations of Hamilton's rule. Here we derive Hamilton's rule with explicit stochasticity, leading to new predictions about the evolution of altruism. We show that altruists can increase the long-term success of their genotype...

Ecology, Jan 12, 2018

Cooperative breeding decreases the direct reproductive output of subordinate individuals, but coo... more Cooperative breeding decreases the direct reproductive output of subordinate individuals, but cooperation can be evolutionarily favored when there are challenges or constraints to breeding independently. Environmental factors, including temperature, precipitation, latitude, high seasonality and environmental harshness have been hypothesized to correlate with the presence of cooperative breeding. However, to test the relationship between cooperation and ecological constraints requires comparative data on the frequency and variation of cooperative breeding across differing environments, ideally replicated across multiple species. Paper wasps are primitively social species, forming colonies composed of reproductively active dominants and foraging subordinates. Adult female wasps, referred to as foundresses, initiate new colonies. Nests can be formed by a single solitary foundress (non-cooperative) or by multiple foundress associations (cooperative). Cooperative behavior varies within a...

Genome biology and evolution, Jan 26, 2017

Life-history transitions require major reprogramming at the behavioural and physiological level. ... more Life-history transitions require major reprogramming at the behavioural and physiological level. Mating and reproductive maturation are known to trigger changes in gene transcription in reproductive tissues in a wide range of organisms, but we understand little about the molecular consequences of a failure to mate or become reproductively mature, and it is not clear to what extent these processes trigger neural as well as physiological changes. In this study we examined the molecular processes underpinning the behavioural changes that accompany the major life-history transitions in a key pollinator, the bumblebee Bombus terrestris. We compared neuro-transcription in queens that succeeded or failed in switching from virgin and immature states, to mated and reproductively mature states. Both successes and failures were associated with distinct molecular profiles, illustrating how development during adulthood triggers distinct molecular profiles within a single caste of a eusocial inse...

Proceedings. Biological sciences / The Royal Society, Jan 22, 2014

Division of labour is central to the ecological success of eusocial insects, yet the evolutionary... more Division of labour is central to the ecological success of eusocial insects, yet the evolutionary factors driving increases in complexity in division of labour are little known. The size-complexity hypothesis proposes that, as larger colonies evolve, both non-reproductive and reproductive division of labour become more complex as workers and queens act to maximize inclusive fitness. Using a statistically robust phylogenetic comparative analysis of social and environmental traits of species within the ant tribe Attini, we show that colony size is positively related to both non-reproductive (worker size variation) and reproductive (queen-worker dimorphism) division of labour. The results also suggested that colony size acts on non-reproductive and reproductive division of labour in different ways. Environmental factors, including measures of variation in temperature and precipitation, had no significant effects on any division of labour measure or colony size. Overall, these results s...

PeerJ, 2015

Insects have been used as an exemplary model in studying longevity, from extrinsic mortality pres... more Insects have been used as an exemplary model in studying longevity, from extrinsic mortality pressures to intrinsic senescence. In the highly eusocial insects, great degrees of variation in lifespan exist between morphological castes in relation to extreme divisions of labour, but of particular interest are the primitively eusocial insects. These species represent the ancestral beginnings of eusociality, in which castes are flexible and based on behaviour rather than morphology. Here we present data on the longevity of the primitively eusocial Neotropical paper wasp P. canadensis, in a captive setting removed of environmental hazards. Captive Polistes canadensis had an average lifespan of 193 ± 10.5 days; although this average is shorter than most bee and ant queens, one individual lived for 506 days in the lab-longer than most recorded wasps and bees. Natal colony variation in longevity does exist between P. canadensis colonies, possibly due to nutritional and genetic factors. This study provides a foundation for future investigations on the effects of intrinsic and extrinsic factors on longevity in primitively eusocial insects, as well as the relationship with natal group and cohort size.

Genome biology and evolution, Jan 19, 2014

Many organisms can generate alternative phenotypes from the same genome, enabling individuals to ... more Many organisms can generate alternative phenotypes from the same genome, enabling individuals to exploit diverse and variable environments. A prevailing hypothesis is that such adaptation has been favored by gene duplication events, which generate redundant genomic material that may evolve divergent functions. Vertebrate examples of recent whole-genome duplications are sparse although one example is the salmonids, which have undergone a whole-genome duplication event within the last 100 Myr. The life-cycle of the Atlantic salmon, Salmo salar, depends on the ability to produce alternating phenotypes from the same genome, to facilitate migration and maintain its anadromous life history. Here, we investigate the hypothesis that genome-wide and local gene duplication events have contributed to the salmonid adaptation. We used high-throughput sequencing to characterize the transcriptomes of three key organs involved in regulating migration in S. salar: Brain, pituitary, and olfactory epi...

Ecology and Evolution, 2012

Climate has long been suggested to affect population genetic structures of eusocial insect societ... more Climate has long been suggested to affect population genetic structures of eusocial insect societies. For instance, Hamilton [Journal of Theoretical Biology 7 (1964) 17] discusses whether temperate and tropical eusocial insects may show differences in population-level genetic structure and viscosity, and how this might relate to differences in the degree of synchrony in their life cycles or modes of nest founding. Despite the importance of Hamilton's 1964 papers, this specific idea has not been tested in actual populations of wasps, probably due to the paucity of studies on tropical species. Here, we compare colony and population genetic structures in two species of primitively eusocial paper wasps with contrasting ecologies: the tropical species Polistes canadensis and the temperate species P. dominulus. Our results provide important clarifications of Hamilton's discussion. Specifically, we show that the genetic structures of the temperate and tropical species were very similar, indicating that seasonality does not greatly affect population viscosity or inbreeding. For both species, the high genetic differentiation between nests suggests strong selection at the nest level to live with relatives, whereas low population viscosity and low genetic differentiation between nest aggregations might reflect balancing selection to disperse, avoiding competition with relatives. Overall, our study suggests no prevalence of seasonal constraints of the life cycle in affecting the population genetic structure of eusocial paper wasps. These conclusions are likely to apply also to other primitively eusocial insects, such as halictine bees. They also highlight how selection for a kin structure that promotes altruism can override potential effects of ecology in eusocial insects.

New Scientist, 2012

ABSTRACT Cells and insects seem to inhabit different worlds, but they seem to be linked at a deep... more ABSTRACT Cells and insects seem to inhabit different worlds, but they seem to be linked at a deep organisational level

Proceedings of the Royal Society B: Biological Sciences, 2006

Understanding how a single genome can produce a variety of different phenotypes is of fundamental... more Understanding how a single genome can produce a variety of different phenotypes is of fundamental importance in evolutionary and developmental biology. One of the most striking examples of phenotypic plasticity is the female caste system found in eusocial insects, where variation in reproductive (queens) and non-reproductive (workers) phenotypes results in a broad spectrum of caste types, ranging from behavioural through to morphological castes. Recent advances in genomic techniques allow novel comparisons on the nature of caste phenotypes to be made at the level of the genes in organisms for which there is little genome information, facilitating new approaches in studying social evolution and behaviour. Using the paper waspPolistes canadensisas a model system, we investigated for the first time how behavioural castes in primitively eusocial insect societies are associated with differential expression of shared genes. We found that queens and newly emerged females express gene expre...

Proceedings of the National Academy of Sciences, 2003

Division of labor is fundamental to the success of all societies. The most striking examples are ... more Division of labor is fundamental to the success of all societies. The most striking examples are the physically polymorphic worker castes in social insects with clear morphological adaptations to different roles. These polymorphic worker castes have previously been thought to be a classic example of nongentically controlled polymorphism, being mediated entirely by environmental cues. Here we show that worker caste development in the leaf-cutting ant Acromyrmex echinatior has a significant genetic component. Individuals of different patrilines within the same colony differ in their propensities to develop into minor or major workers. The mechanism appears to be plastic, with caste destiny resulting from interplay between nurture and nature. Unlike the few other recently discovered examples of a genetic influence on caste determination, the present result does not relate to any rare or exceptional circumstances, such as interspecific hybridization. The results suggest that a significa...

Nature, 2000

An unresolved issue in cortical development concerns the relative contributions of intrinsic and ... more An unresolved issue in cortical development concerns the relative contributions of intrinsic and extrinsic factors to the functional speci®cation of different cortical areas 1±4. Ferrets in which retinal projections are redirected neonatally to the auditory thalamus 5

Insectes Sociaux, 2004

Emery's rule predicts that social parasites and their hosts share common ancestry and are therefo... more Emery's rule predicts that social parasites and their hosts share common ancestry and are therefore likely to be close relatives. Within the leaf-cutting ant genus Acromyrmex, two taxa of social parasites have been found, which are thought to occupy opposite grades of permanent social parasitism, based on their contrasting morphologies: Acromyrmex insinuator differs little in morphology from its freeliving congeneric host species and produces a worker caste, and is thus thought to represent an early grade of social parasitism. At the other extreme, Pseudoatta spp. exhibit a very specialised morphology and lack a worker caste, both of which are characteristics of an evolutionarily derived grade of social parasitism. Here we present a molecular phylogeny using partial sequences of cytochrome oxidase I and II of about half of the known Acromyrmex species including two social parasites, their hosts and all congeneric species occurring sympatrically. We show that the two inquiline parasites represent two separate origins of social parasitism in the genus Acromyrmex. The early-grade social parasite A. insinuator is highly likely to be the sister species of its host Acromyrmex echinator, but the derived social parasite Pseudoatta sp. is not the sister species of its extant host Acromyrmex rugosus.

Current Opinion in Cell Biology, 2012

Epigenetic modifications are ancient and widely utilised mechanisms that have been recruited acro... more Epigenetic modifications are ancient and widely utilised mechanisms that have been recruited across fungi, plants and animals for diverse but fundamental biological functions, such as cell differentiation. Recently, a functional DNA methylation system was identified in the honeybee, where it appears to underlie queen and worker caste differentiation. This discovery, along with other insights into the epigenetics of social insects, allows provocative analogies to be drawn between insect caste differentiation and cellular differentiation, particularly in mammals. Developing larvae in social insect colonies are totipotent: they retain the ability to specialise as queens or workers, in a similar way to the totipotent cells of early embryos before they differentiate into specific cell lineages. Further, both differentiating cells and insect castes lose phenotypic plasticity by committing to their lineage, losing the ability to be readily reprogrammed. Hence, a comparison of the epigenetic mechanisms underlying lineage differentiation (and reprogramming) between cells and social insects is worthwhile. Here we develop a conceptual model of how loss and regain of phenotypic plasticity might be conserved for individual specialisation in both cells and societies. This framework forges a novel link between two fields of biological research, providing predictions for a unified approach to understanding the molecular mechanisms underlying biological complexity.

Current Biology, 2008

Differences in brain gene expression between sleep and waking as revealed by mRNA differential di... more Differences in brain gene expression between sleep and waking as revealed by mRNA differential display and cDNA microarray technology. J. Sleep Res. 8 (Suppl. 1), 44-52.