Jacobus Boomsma - Academia.edu (original) (raw)

Papers by Jacobus Boomsma

FEMS Microbiology Ecology

Rhizobiales are well-known plant-root nitrogen-fixing symbionts, but the functions of insect-asso... more Rhizobiales are well-known plant-root nitrogen-fixing symbionts, but the functions of insect-associated Rhizobiales are poorly understood. We obtained genomes of three strains associated with Acromyrmex leaf-cutting ants and show that, in spite of being extracellular gut symbionts, they lost all pathways for essential amino acid biosynthesis, making them fully dependent on their hosts. Comparison with 54 Rhizobiales genomes showed that all insect-associated Rhizobiales lost the ability to fix nitrogen and that the Acromyrmex symbionts had exceptionally also lost the urease genes. However, the Acromyrmex strains share biosynthesis pathways for riboflavin vitamin, queuosine and a wide range of antioxidant enzymes likely to be beneficial for the ant fungus-farming symbiosis. We infer that the Rhizobiales symbionts catabolize excess of fungus-garden-derived arginine to urea, supplementing complementary Mollicutes symbionts that turn arginine into ammonia and infer that these combined sy...

Ant colonies are higher-level organisms consisting of specialized reproductive and non-reproducti... more Ant colonies are higher-level organisms consisting of specialized reproductive and non-reproductive individuals that differentiate early in development, similar to germ-soma segregation in bilateral Metazoa. Analogous to diverging cell lines, developmental differentiation of individual ants has often been considered in epigenetic terms, but the sets of genes that determine caste phenotypes throughout larval and pupal development remain unknown. Here we reconstruct the individual developmental trajectories of two ant species after obtaining > 1400 whole-genome transcriptomes. Using a novel backward prediction algorithm, we show that caste phenotypes can be accurately predicted by genome-wide transcriptome profiling. We find that caste differentiation is increasingly canalized from early development onwards, particularly in germline individuals (gynes/queens), and that the juvenile hormone signalling pathway regulates this process with feedback from diverging larval body mass. We q...

Journal of Evolutionary Biology, 2020

Genomic imprinting results in parent‐of‐origin‐dependent gene expression biased towards either th... more Genomic imprinting results in parent‐of‐origin‐dependent gene expression biased towards either the maternally or paternally derived allele at the imprinted locus. The kinship theory of genomic imprinting argues that this unusual expression pattern can be a manifestation of intra‐genomic conflict between the maternally and paternally derived halves of the genome that arises because they are not equally related to the genomes of social partners. The theory thus predicts that imprinting may evolve wherever there are close interactions among asymmetrically related kin. The social Hymenoptera with permanent caste differentiation are suitable candidates for testing the kinship theory because haplodiploid sex determination creates strong relatedness asymmetries and nursing workers interact closely with kin. However, progress in the search for imprinted genes in the social Hymenoptera has been slow, in part because tests for imprinting rely on reciprocal crosses that are impossible in most ...

Molecular & Cellular Proteomics, 2018

Nature Ecology & Evolution, 2018

Specialized queens and lifetime unmated workers evolved once in the common ancestor of all ants, ... more Specialized queens and lifetime unmated workers evolved once in the common ancestor of all ants, but whether caste development across ants continues to be at least partly regulated by a single core set of genes remains obscure. We analysed brain transcriptomes from five ant species (three subfamilies) and reconstructed the origins of genes with caste-biased expression. Ancient genes predating the Neoptera were more likely to regulate gyne (virgin queen) phenotypes, while caste differentiation roles of younger, ant-lineage-specific genes varied. Transcriptome profiling showed that the ancestral network for caste-specific gene-regulation has been maintained, but that signatures of common ancestry are obscured by later modifications. Adjusting for such differences, we identified a core gene-set that: 1. consistently displayed similar directions and degrees of caste-differentiated expression, and 2. have mostly not been reported as being involved in caste differentiation. These core regulatory genes exist in the genomes of ant species that secondarily lost the queen caste, but expression differences for reproductive and sterile workers are minor and similar to social paper wasps that lack differentiated castes. Many caste-biased ant genes have caste-differentiated expression in honeybees, but directions of caste bias were uncorrelated, as expected when permanent castes evolved independently in both lineages. Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:

Biological reviews of the Cambridge Philosophical Society, Jan 15, 2017

More than a century ago, William Morton Wheeler proposed that social insect colonies can be regar... more More than a century ago, William Morton Wheeler proposed that social insect colonies can be regarded as superorganisms when they have morphologically differentiated reproductive and nursing castes that are analogous to the metazoan germ-line and soma. Following the rise of sociobiology in the 1970s, Wheeler's insights were largely neglected, and we were left with multiple new superorganism concepts that are mutually inconsistent and uninformative on how superorganismality originated. These difficulties can be traced to the broadened sociobiological concept of eusociality, which denies that physical queen-worker caste differentiation is a universal hallmark of superorganismal colonies. Unlike early evolutionary naturalists and geneticists such as Weismann, Huxley, Fisher and Haldane, who set out to explain the acquisition of an unmated worker caste, the goal of sociobiology was to understand the evolution of eusociality, a broad-brush convenience category that covers most forms o...

Oikos, 2015

Several decades of research in humans, other vertebrates, and social insects have offered fascina... more Several decades of research in humans, other vertebrates, and social insects have offered fascinating insights into the dynamics of punishment (and its subset, policing), but authors have only rarely addressed whether there are fundamental joint principles underlying the maintenance of these behaviors. Here we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punishing roles in animal societies. We apply our scheme to societies of eusocial Hymenoptera and nonhuman vertebrate social breeders, and we outline potential extensions for understanding conflict regulation among cells in metazoan bodies and unrelated individuals in human societies. We highlight that: 1) no social unit is expected to express punishment behavior unless it collects positive inclusive fitness benefits that surpass alternative benefits of bystanding; 2) punishment with public good benefits can be maintained through either direct fitness benefits (coercion) or indirect fitness benefits (correction) or both; 3) differences across social systems in the distributions of power, relatedness, and reproductive options drive variation in the extent to which individuals actively punish; and 4) inclusive fitness logic captures many punishment-relevant evolutionary and ecological variables in a single framework that appears to apply across very different types of social arrangements.

Bacterial symbionts are important fitness determinants of insects. Some hosts have independently ... more Bacterial symbionts are important fitness determinants of insects. Some hosts have independently acquired microbes of the same lineage to meet similar challenges, but whether distantly related hosts that live in symbiosis can maintain similar microbial communities has not been investigated. The varying degrees of nest-sharing between Megalomyrmex social parasites (Solenopsidini) and their fungus-growing ant hosts (Attini) allowed us to address this question, as both ant lineages rely on the same fungal diet, interact through a variety of parasitic relationships, and are distantly related. We used tag-encoded FLX 454 pyrosequencing and diagnostic PCR to map bacterial symbiont diversity across the Megalomyrmex phylogenetic tree, which also contains clades of freeliving generalist predators. We show that social parasites sharing the nest with their hosts or merely consuming host brood and fungus garden, harbour microbial communities that are partially overlapping with those of the attine species that they exploit. Particularly abundant were Entomoplasmatales, Bartonellaceae, Acinetobacter, Wolbachia and Pseudonocardia, in many cases co-infecting associated hosts and parasites with identical 16S rRNA genotypes. We further reconstructed population level infection dynamics for Entomoplasmatales and Bartonellaceae species in the particularly well sampled species-pair of M. symmetochus guest ants and Sericomyrmex amabilis hosts. Our results suggest that hosts and socially parasitic Megalomyrmex ants share a number of prevalent bacterial symbionts, as these bacteria may be transmitted via consumption of shared fungus gardens, predation on host brood by the social parasites, or parasite grooming by host workers.

Bmc Evolutionary Biology, 2004

Background: Parasite heterogeneity and within-host competition are thought to be important factor... more Background: Parasite heterogeneity and within-host competition are thought to be important factors influencing the dynamics of host-parasite relationships. Yet, while there have been many theoretical investigations of how these factors may act, empirical data is more limited. We investigated the effects of parasite density and heterogeneity on parasite virulence and fitness using four strains of the entomopathogenic fungus, Metarhizium anisopliae var. anisopliae, and its leafcutting ant host Acromyrmex echinatior as the model system. Results: The relationship between parasite density and infection was sigmoidal, with there being an invasion threshold for an infection to occur (an Allee effect). Although spore production was positively density-dependent, parasite fitness decreased with increasing parasite density, indicating within-host scramble competition. The dynamics differed little between the four strains tested. In mixed infections of three strains the infection-growth dynamics were unaffected by parasite heterogeneity. Conclusions: The strength of within-host competition makes dispersal the best strategy for the parasite. Parasite heterogeneity may not have effected virulence or the infection dynamics either because the most virulent strain outcompeted the others, or because the interaction involved scramble competition that was impervious to parasite heterogeneity. The dynamics observed may be common for virulent parasites, such as Metarhizium, that produce aggregated transmission stages. Such parasites make useful models for investigating infection dynamics and the impact of parasite competition.

Proceedings of the Royal Society B: Biological Sciences, 2009

Theory predicts that altruism is only evolutionarily stable if it is preferentially directed towa... more Theory predicts that altruism is only evolutionarily stable if it is preferentially directed towards relatives, so that any such behaviour towards seemingly unrelated individuals requires scrutiny. Queenless army ant colonies, which have anecdotally been reported to fuse with queenright foreign colonies, are such an enigmatic case. Here we combine experimental queen removal with population genetics and cuticular chemistry analyses to show that colonies of the African army antDorylus molestusfrequently merge with neighbouring colonies after queen loss. Merging colonies often have no direct co-ancestry, but are on average probably distantly related because of overall population viscosity. The alternative of male production by orphaned workers appears to be so inefficient that residual inclusive fitness of orphaned workers might be maximized by indiscriminately merging with neighbouring colonies to increase their reproductive success. We show that worker chemical recognition profiles r...

Proceedings of the Royal Society of London. Series B: Biological Sciences, 2000

Ants provide excellent opportunities for studying the evolutionary aspects of reproductive con£ic... more Ants provide excellent opportunities for studying the evolutionary aspects of reproductive con£ict. Relatedness asymmetries owing to the haplodiploid sex determination of Hymenoptera create substantial ¢tness incentives for gaining control over sex allocation, often at the expense of the ¢tness interests of nest-mates. Under worker-controlled split sex ratios either the reproductive interests of the mother queen (when workers male bias the sex ratio) or the father (when workers female bias the sex ratio), but never that of both parents simultaneously, are ful¢lled. When workers bias sex ratios according to the frequency of queen mating, males which co-sire a colony have a joint interest in manipulating their daughter workers into rearing a more female-biased sex ratio. Here we show that males of the ant Formica truncorum achieve such manipulation by partial sperm clumping, so that the cohort-speci¢c relatedness asymmetry of the workers in colonies with multiple fathers is higher than the cumulative relatedness asymmetry across worker cohorts. This occurs because a single male fathers the majority of the o¡spring within a cohort. Colonies with higher average cohort-speci¢c relatedness asymmetry produce more female-biased sex ratios. Posthumously expressed male genes are thus able to oppose the reproductive interests of the genes expressed in queens and the latter apparently lack mechanisms for enforcing full control over sperm mixing and sperm allocation.

Proceedings of the Royal Society of London. Series B: Biological Sciences, 2004

Proceedings of the National Academy of Sciences, 2008

Social groups are vulnerable to cheating because the reproductive interests of group members are ... more Social groups are vulnerable to cheating because the reproductive interests of group members are rarely identical. All cooperative systems are therefore predicted to involve a mix of cooperative and cheating genotypes, with the frequency of the latter being constrained by the suppressive abilities of the former. The most significant potential conflict in social insect colonies is over which individuals become reproductive queens rather than sterile workers. This reproductive division of labor is a defining characteristic of eusocial societies, but individual larvae will maximize their fitness by becoming queens whereas their nestmates will generally maximize fitness by forcing larvae to become workers. However, evolutionary constraints are thought to prevent cheating by removing genetic variation in caste propensity. Here, we show that one-fifth of leaf-cutting ant patrilines cheat their nestmates by biasing their larval development toward becoming queens rather than workers. Two di...

Philosophical Transactions of the Royal Society B: Biological Sciences, 2009

All evidence currently available indicates that obligatory sterile eusocial castes only arose via... more All evidence currently available indicates that obligatory sterile eusocial castes only arose via the association of lifetime monogamous parents and offspring. This is consistent with Hamilton's rule (brs>roc), but implies that relatedness cancels out of the equation because average relatedness to siblings (rs) and offspring (ro) are both predictably 0.5. This equality implies that any infinitesimally small benefit of helping at the maternal nest (b), relative to the cost in personal reproduction (c) that persists throughout the lifespan of entire cohorts of helpers suffices to establish permanent eusociality, so that group benefits can increase gradually during, but mostly after the transition. The monogamy window can be conceptualized as a singularity comparable with the single zygote commitment of gametes in eukaryotes. The increase of colony size in ants, bees, wasps and termites is thus analogous to the evolution of multicellularity. Focusing on lifetime monogamy as a un...

Naturwissenschaften, 2003

Molecular Ecology, 2010

Altruism in social insects has evolved between closely related full-siblings. It is therefore of ... more Altruism in social insects has evolved between closely related full-siblings. It is therefore of considerable interest why some groups have secondarily evolved low within-colony relatedness, which in turn affects the relatedness incentives of within-colony cooperation and conflict. The highest queen mating frequencies, and therefore among the lowest degrees of colony relatedness, occur in Apis honeybees and army ants of the subfamilies Aenictinae, Ecitoninae, and Dorylinae, suggesting that common life history features such as reproduction by colony fission and male biased numerical sex-ratios have convergently shaped these mating systems. Here we show that ponerine army ants of the genus Simopelta, which are distantly related but similar in general biology to other army ants, have strictly monandrous queens. Preliminary data suggest that workers reproduce in queenright colonies, which is in sharp contrast to other army ants. We hypothesize that differences in mature colony size and social complexity may explain these striking discrepancies.

Molecular Ecology, 2011

Sperm competition can produce fascinating adaptations with far-reaching evolutionary consequences... more Sperm competition can produce fascinating adaptations with far-reaching evolutionary consequences. Social taxa make particularly interesting models, because the outcome of sexual selection determines the genetic composition of groups, with attendant sociobiological consequences. Here, we use molecular tools to uncover some of the mechanisms and consequences of sperm competition in the leaf-cutting ant Atta colombica, a species with extreme worker size polymorphism. Competitive PCR allowed quantification of the relative numbers of sperm stored by queens from different males, and offspring genotyping revealed how sperm number translated into paternity of eggs and adult workers. We demonstrate that fertilization success is directly related to sperm numbers, that stored sperm are well-mixed and that egg paternity is constant over time. Moreover, worker size was found to have a considerable genetic component, despite expectations that genetic effects on caste fate should be minor in species with a low degree of polyandry. Our data suggest that sexual conflict over paternity is largely resolved by the lifetime commitment between mates generated by long-term sperm storage, and show that genetic variation for caste can persist in societies with comparatively high relatedness.

Journal of Theoretical Biology, 1997

Using inclusive fitness models, this study determines the optimal patterns of split-sex-ratio all... more Using inclusive fitness models, this study determines the optimal patterns of split-sex-ratio allocation for hymenopteran workers when colonies have a single queen, and queens mate with either one or two males. This particular colony kin-structure is common in social Hymenoptera. Importantly, the basic split-sex-ratio pattern of allocation, with some colonies producing exclusively or largely males and the others producing exclusively or largely queens, is shown to be robust with respect to the parameters investigated: errors in the assessment of queen mating frequency by workers, male-production by workers, unequal male contributions to paternity in double-mated queens, and partial queen control. Conditions under which split sex ratios are not expected, or may be non-extreme, are discussed.

Journal of Invertebrate Pathology, 2004

We investigated the prevalence of entomopathogenic fungi associated with leaf-cutting ant colonie... more We investigated the prevalence of entomopathogenic fungi associated with leaf-cutting ant colonies in a small area of tropical forest in Panama. There was a high abundance of Metarhizium anisopliae var. anisopliae near the colonies. Beauveria bassiana was also detected in the soil, Aspergillus flavus in dump material, and six Camponotus atriceps ants were found infected with Cordyceps sp.. Based on a partial sequence of the IGS region, almost all of the M. anisopliae var. anisopliae isolates fell within one of the three main clades of M. anisopliae var. anisopliae, but with there still being considerable diversity within this clade. The vast majority of leaf-cutting ants collected were not infected by any entomopathogenic fungi. While leaf-cutting ants at this site must, therefore, regularly come into contact with a diversity of entomopathogenic fungi, they do not appear to be normally infected by them.