scholarly journals Evidence for a conserved queen-worker genetic toolkit across slave-making ants and their ant hosts

2021 ◽  
Author(s):  
Barbara Feldmeyer ◽  
Claudia Gstoettl ◽  
Jennifer Wallner ◽  
Evelien Jongepier ◽  
Alice Seguret ◽  
...  
Keyword(s):  
Division Of Labour ◽  
Social Parasites ◽  
Social Hymenoptera ◽  
Strong Connectivity ◽  
Core Set ◽  
Parasitic Lifestyle ◽  
Ecological Success ◽  
Worker Caste ◽  
Caste Differences ◽  
Genetic Toolkit

The ecological success of social Hymenoptera (ants, bees, wasps) depends on the division of labour between the queen and workers. Each caste is highly specialized in their respective function in morphology, behaviour and life history traits, such as lifespan and fecundity. Despite strong defences against alien intruders, insect societies are vulnerable to social parasites, such as workerless inquilines or slave-making (dulotic) ants. Here, we investigate whether gene expression varies in parallel ways between slave-making ants and their host ants across five independent origins of ant slavery in the Formicoxenus-group of the ant tribe Crematogastrini. As caste differences are often less pronounced in slave-making ants than non-parasitic ants, we also compare the transcriptomes of queens and workers in these species. We demonstrate a substantial overlap in expression differences between queens and workers across taxa, irrespective of lifestyle. Caste affects the transcriptomes much more profoundly than lifestyle, as indicated by 37 times more genes being linked to caste than to lifestyle and by multiple caste-associated gene modules with strong connectivity. However, several genes and one gene module are linked to the slave-making lifestyle across the independent origins, pointing to some evolutionary convergence. Finally, we do not find evidence for an interaction between caste and lifestyle, indicating that caste differences remain consistent even when species switch to a parasitic lifestyle. Our findings are a strong indication for the existence of a core set of genes whose expression is linked to the queen and worker caste in this ant taxon, supporting the genetic-toolkit hypothesis.

scholarly journals Phylogenetic tests reject Emery's rule in the evolution of social parasitism in yellowjackets and hornets (Hymenoptera: Vespidae, Vespinae)

2015 ◽  
Vol 2 (9) ◽  
pp. 150159 ◽  
Author(s):  
Federico Lopez-Osorio ◽  
Adrien Perrard ◽  
Kurt M. Pickett ◽  
James M. Carpenter ◽  
Ingi Agnarsson
Keyword(s):  
Host Species ◽  
Phylogenetic Analyses ◽  
Social Parasitism ◽  
Strict Sense ◽  
Brood Care ◽  
Social Parasites ◽  
Social Hymenoptera ◽  
The Social ◽  
Different Types ◽  
Worker Caste

Social parasites exploit the brood-care behaviour and social structure of one or more host species. Within the social Hymenoptera there are different types of social parasitism. In its extreme form, species of obligate social parasites, or inquilines, do not have the worker caste and depend entirely on the workers of a host species to raise their reproductive offspring. The strict form of Emery's rule states that social parasites share immediate common ancestry with their hosts. Moreover, this rule has been linked with a sympatric origin of inquilines from their hosts. Here, we conduct phylogenetic analyses of yellowjackets and hornets based on 12 gene fragments and evaluate competing evolutionary scenarios to test Emery's rule. We find that inquilines, as well as facultative social parasites, are not the closest relatives of their hosts. Therefore, Emery's rule in its strict sense is rejected, suggesting that social parasites have not evolved sympatrically from their hosts in yellowjackets and hornets. However, the relaxed version of the rule is supported, as inquilines and their hosts belong to the same Dolichovespula clade. Furthermore, inquilinism has evolved only once in Dolichovespula .

scholarly journals Recombination mapping of the Brazilian stingless bee Frieseomelitta varia confirms high recombination rates in social hymenoptera

BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Prashant Waiker ◽  
Fabiano Carlos Pinto de Abreu ◽  
Danielle Luna-Lucena ◽  
Flávia Cristina Paula Freitas ◽  
Zilá Luz Paulino Simões ◽  
...  
Keyword(s):  
Linkage Map ◽  
Social Evolution ◽  
Stingless Bee ◽  
Recombination Rates ◽  
Social Hymenoptera ◽  
Social Species ◽  
A Genome ◽  
Study Results ◽  
Worker Caste ◽  
Genomic Recombination

Abstract Background Meiotic recombination is a fundamental genetic process that shuffles allele combinations and promotes accurate segregation of chromosomes. Analyses of the ubiquitous variation of recombination rates within and across species suggest that recombination is evolving adaptively. All studied insects with advanced eusociality have shown exceptionally high recombination rates, which may represent a prominent case of adaptive evolution of recombination. However, our understanding of the relationship between social evolution and recombination rates is incomplete, partly due to lacking empirical data. Here, we present a linkage map of the monandrous, advanced eusocial Brazilian stingless bee, Frieseomelitta varia, providing the first recombination analysis in the diverse Meliponini (Hymenoptera, Apidae). Results Our linkage map includes 1417 markers in 19 linkage groups. This map spans approximately 2580 centimorgans, and comparisons to the physical genome assembly indicate that it covers more than 75 % of the 275 Megabasepairs (Mbp) F. varia genome. Thus, our study results in a genome-wide recombination rate estimate of 9.3–12.5 centimorgan per Mbp. This value is higher than estimates from nonsocial insects and comparable to other highly social species, although it does not support our prediction that monandry and strong queen-worker caste divergence of F. varia lead to even higher recombination rates than other advanced eusocial species. Conclusions Our study expands the association between elevated recombination and sociality in the order Hymenoptera and strengthens the support for the hypothesis that advanced social evolution in hymenopteran insects invariably selects for high genomic recombination rates.

scholarly journals The loss of flight in ant workers enabled an evolutionary redesign of the thorax for ground labour

2020 ◽  
Author(s):  
Christian Peeters ◽  
Roberto A. Keller ◽  
Adam Khalife ◽  
Georg Fischer ◽  
Julian Katzke ◽  
...  
Keyword(s):  
Central Place ◽  
Division Of Labour ◽  
The Body ◽  
Selective Pressures ◽  
Muscle Adaptations ◽  
Flight Muscles ◽  
Heavy Loads ◽  
Ecological Dominance ◽  
Worker Caste ◽  
Cuticular Structures

Abstract Background Explanations for the ecological dominance of ants generally focus on the benefits of division of labour and cooperation during foraging. However, the principal innovation of ants relative to their wasp ancestors was the evolution of a new phenotype: a wingless worker caste optimized for ground labour. Ant workers are famous for their ability to lift and carry heavy loads, but we know surprisingly little about the morphological basis of their strength. Here we examine the consequences of the universal loss of flight in ant workers on skeletomuscular adaptations in the thorax for enhanced foraging on six legs. Results Using X-ray microcomputed tomography and 3D segmentation, we compared winged queens and wingless workers in Euponera sikorae (subfamily Ponerinae) and Cataglyphis savignyi (subfamily Formicinae). Workers are characterized by five major changes to their thorax: i) fusion of the articulated flight thorax (queens) into a rigid box optimized to support the muscles that operate the head, legs and abdomen, ii) redesign of internal cuticular structures for better bracing and muscle attachment, iii) substantial enlargement of the neck muscles for suspending and moving the head, iv) lengthening of the external trochanter muscles, predominant for the leg actions that lift the body off the ground, v) modified angle of the petiole muscles that are key for flexion of the abdomen. We measured volumes and pennation angles for a few key muscles to assess their increased efficacy. Our comparisons of additional workers across five genera in subfamilies Dorylinae and Myrmicinae show these modifications in the wingless thorax to be consistent. In contrast, a mutillid wasp showed a different pattern of muscle adaptations as a result of the lack of wing muscles. Conclusions Rather than simply a subtraction of costly flight muscles, we propose the ant worker thorax evolved into a power core underlying stronger mandibles, legs, and sting. This contrasts with solitary flightless insects where the lack of central place foraging generated distinct selective pressures for rearranging the thorax. Stronger emphasis is needed on innovations of social insects as individuals at the phenotypic level to further our understanding of the evolution of social behaviours.

scholarly journals The loss of flight in ant workers enabled an evolutionary redesign of the thorax for ground labour

2020 ◽  
Vol 17 (1) ◽  
Author(s):  
Christian Peeters ◽  
Roberto A. Keller ◽  
Adam Khalife ◽  
Georg Fischer ◽  
Julian Katzke ◽  
...  
Keyword(s):  
Central Place ◽  
Division Of Labour ◽  
The Body ◽  
Selective Pressures ◽  
Muscle Adaptations ◽  
Flight Muscles ◽  
Heavy Loads ◽  
Ecological Dominance ◽  
Worker Caste ◽  
Cuticular Structures

Abstract Background Explanations for the ecological dominance of ants generally focus on the benefits of division of labour and cooperation during foraging. However, the principal innovation of ants relative to their wasp ancestors was the evolution of a new phenotype: a wingless worker caste optimized for ground labour. Ant workers are famous for their ability to lift and carry heavy loads, but we know surprisingly little about the morphological basis of their strength. Here we examine the consequences of the universal loss of flight in ant workers on skeletomuscular adaptations in the thorax for enhanced foraging on six legs. Results Using X-ray microcomputed tomography and 3D segmentation, we compared winged queens and wingless workers in Euponera sikorae (subfamily Ponerinae) and Cataglyphis savignyi (subfamily Formicinae). Workers are characterized by five major changes to their thorax: i) fusion of the articulated flight thorax (queens) into a rigid box optimized to support the muscles that operate the head, legs and abdomen, ii) redesign of internal cuticular structures for better bracing and muscle attachment, iii) substantial enlargement of the neck muscles for suspending and moving the head, iv) lengthening of the external trochanter muscles, predominant for the leg actions that lift the body off the ground, v) modified angle of the petiole muscles that are key for flexion of the abdomen. We measured volumes and pennation angles for a few key muscles to assess their increased efficacy. Our comparisons of additional workers across five genera in subfamilies Dorylinae and Myrmicinae show these modifications in the wingless thorax to be consistent. In contrast, a mutillid wasp showed a different pattern of muscle adaptations resulting from the lack of wing muscles. Conclusions Rather than simply a subtraction of costly flight muscles, we propose the ant worker thorax evolved into a power core underlying stronger mandibles, legs, and sting. This contrasts with solitary flightless insects where the lack of central place foraging generated distinct selective pressures for rearranging the thorax. Stronger emphasis is needed on morphological innovations of social insects to further our understanding of the evolution of social behaviours.

scholarly journals Epigenetics in Social Insects: A New Direction for Understanding the Evolution of Castes

2012 ◽  
Vol 2012 ◽  
pp. 1-11 ◽  
Author(s):  
Susan A. Weiner ◽  
Amy L. Toth
Keyword(s):  
Dna Methylation ◽  
Social Insects ◽  
Differential Methylation ◽  
Caste Determination ◽  
The Social ◽  
Worker Castes ◽  
Regulatory Flexibility ◽  
Worker Caste ◽  
Caste Differences ◽  
Epigenetic Research

Epigenetic modifications to DNA, such as DNA methylation, can expand a genome’s regulatory flexibility, and thus may contribute to the evolution of phenotypic plasticity. Recent work has demonstrated the importance of DNA methylation in alternative queen and worker “castes” in social insects, particularly honeybees. Social insects are an excellent system for addressing questions about epigenetics and evolution because: (1) they have dramatic caste polyphenisms that appear to be tied to differential methylation, (2) DNA methylation is widespread in various groups of social insects, and (3) there are intriguing connections between the social environment and DNA methylation in many species, from insects to mammals. In this article, we review research on honeybees, and, when available, other social insects, on DNA methylation and queen and worker caste differences. We outline a conceptual framework for the effects of methylation on caste determination in honeybees that may help guide studies of epigenetic regulation in other polyphenic taxa. Finally, we suggest future paths of study for social insect epigenetic research, including the importance of comparative studies of DNA methylation on a broader range of species, and highlight some key unanswered mechanistic questions about how DNA methylation affects gene regulation.

scholarly journals Cuckoo male bumblebees perform slower and longer flower visits than free-living male and worker bumblebees

2021 ◽  
Vol 151 ◽  
Author(s):  
Alessandro Fisogni ◽  
Gherardo Bogo ◽  
François Massol ◽  
Laura Bortolotti ◽  
Marta Galloni
Keyword(s):  
Colony Development ◽  
Social Parasites ◽  
Free Living ◽  
Mating Period ◽  
Plant Reproductive Success ◽  
Gentiana Lutea ◽  
Whole Plant ◽  
Plant Level ◽  
Flower Visiting ◽  
Worker Caste

Cuckoo bumblebees are a monophyletic group within the genus Bombus and social parasites of free-living bumblebees, upon which they rely to rear their offspring. Cuckoo bumblebees lack the worker caste and visit flowers primarily for their own sustenance and do not collect pollen. Although different flower-visiting behaviours can be expected between cuckoo and free-living bumblebees due to different biological constraints, no study has yet quantified such differences. Here, we provide the first empirical evidence of different flower-visiting behaviours between cuckoo and free-living bumblebees. We recorded the flower-visiting behaviour of 350 individual bumblebees over two years in a wild population of the entomophilous plant Gentiana lutea, of which they are among the main pollinators. In cuckoo bumblebees (28.9% of the total), we only found males, while we found both workers and males in free-living bumblebees. Cuckoo bumblebees visited significantly more flowers for longer time periods than both free-living bumblebee workers and males within whorls, while differences at the whole-plant level were less marked. Free-living bumblebee males visited more flowers and performed slightly longer flower visits than workers. Behavioural differences between cuckoo male bumblebees and free-living bumblebee workers are likely related to different foraging needs, while differences between cuckoo and free-living bumblebee males may be caused by differences in colony development and a delayed mating period of free-living bumblebees. The longer visits made by cuckoo male bumblebees will likely negatively affect plant reproductive success through increased within-plant pollen flow.

scholarly journals Morphological evolution in the ant reproductive caste

2020 ◽  
Author(s):  
Raquel Divieso ◽  
Thiago S. R. Silva ◽  
Marcio R. Pie
Keyword(s):  
Body Size ◽  
Morphological Variation ◽  
Morphological Evolution ◽  
Division Of Labour ◽  
Comprehensive Treatment ◽  
Size Distributions ◽  
Reproductive Division Of Labour ◽  
Evolution Of Eusociality ◽  
Worker Caste ◽  
Reproductive Division

AbstractThe evolution of eusociality led to severe changes in the general hymenopteran body plan. In particular, the evolution of reproductive division of labour caused the worker caste to be largely freed from the demands involved in reproduction. As a consequence, workers were able to evolve highly specialized morphologies for foraging and colony maintenance, whereas the reproductive caste became specialized for reproduction. Despite these important changes, little is known about general patterns of morphological evolution within the ant reproductive caste. Our goals were to characterize morphological variation in the ant reproductive caste and to test whether different sexes display variation in their evolutionary rates. We obtained measurements of 897 specimens from a total of 678 ant species. The shapes of the size distributions were similar between sexes, with queens being larger than males in all traits except for eye length. Contrary to the expectation based on Rensch’s rule, although queens were larger, the degree of dimorphism increased with body size. Finally, there is strong evidence for an accelerated tempo of morphological evolution in queens in relation to males. These results represent the first comprehensive treatment of morphological variation in the ant reproductive caste and provide important new insights into their evolution.

scholarly journals Two new species of socially parasitic Nylanderia ants from the southeastern United States

ZooKeys ◽  
2020 ◽  
Vol 921 ◽  
pp. 23-48
Author(s):  
Steven J. Messer ◽  
Stefan P. Cover ◽  
Christian Rabeling
Keyword(s):  
United States ◽  
Life History ◽  
New Species ◽  
Southeastern United States ◽  
Social Parasitism ◽  
Life History Strategies ◽  
Social Parasite ◽  
Social Parasites ◽  
Two New Species ◽  
Worker Caste

In ants, social parasitism is an umbrella term describing a variety of life-history strategies, where a parasitic species depends entirely on a free-living species, for part of or its entire life-cycle, for either colony founding, survival, and/or reproduction. The highly specialized inquiline social parasites are fully dependent on their hosts for their entire lifecycles. Most inquiline species are tolerant of the host queen in the parasitized colony, forgo producing a worker caste, and invest solely in the production of sexual offspring. In general, inquilines are rare, and their geographic distribution is limited, making it difficult to study them. Inquiline populations appear to be small, cryptic, and they are perhaps ephemeral. Thus, information about their natural history is often fragmentary or non-existent but is necessary for understanding the socially parasitic life history syndrome in more detail. Here, we describe two new species of inquiline social parasites, Nylanderia deyrupisp. nov. and Nylanderia parasiticasp. nov., from the southeastern United States, parasitizing Nylanderia wojciki and Nylanderia faisonensis, respectively. The formicine genus Nylanderia is large and globally distributed, but until the recent description of Nylanderia deceptrix, social parasites were unknown from this genus. In addition to describing the new social parasite species, we summarize the fragmentary information known about their biology, present a key to both the queens and the males of the Nylanderia social parasites, and discuss the morphology of the social parasites in the context of the inquiline syndrome.

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

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Daniel Elsner ◽  
Klaus Hartfelder ◽  
Judith Korb
Keyword(s):  
Molecular Mechanisms ◽  
Storage Proteins ◽  
Division Of Labour ◽  
Social Hymenoptera ◽  
Evolutionary Transitions ◽  
Macrotermes Bellicosus ◽  
Reproductive Division Of Labour ◽  
Multicellular Organisms ◽  
Reproductive Division ◽  
Task Division

AbstractDivision 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.

scholarly journals The loss of flight in ant workers enabled an evolutionary redesign of the thorax for ground labour

2020 ◽  
Author(s):  
Christian Peeters ◽  
Roberto A. Keller ◽  
Adam Khalife ◽  
Georg Fischer ◽  
Julian Katzke ◽  
...  
Keyword(s):  
Central Place ◽  
Division Of Labour ◽  
The Body ◽  
Selective Pressures ◽  
Muscle Adaptations ◽  
Flight Muscles ◽  
Heavy Loads ◽  
Ecological Dominance ◽  
Worker Caste ◽  
Cuticular Structures

Abstract Background Explanations for the ecological dominance of ants generally focus on the benefits of division of labour and cooperation during foraging. However, the principal innovation of ants relative to their wasp ancestors was the evolution of a new phenotype: a wingless worker caste optimized for ground labour. Ant workers are famous for their ability to lift and carry heavy loads, but we know surprisingly little about the morphological basis of their strength. Here we examine the consequences of the universal loss of flight in ant workers on skeletomuscular adaptations in the thorax for enhanced foraging on six legs. Results Using X-ray microcomputed tomography and 3D segmentation, we compared winged queens and wingless workers in Euponera sikorae (subfamily Ponerinae) and Cataglyphis savignyi (subfamily Formicinae). Workers are characterized by five major changes to their thorax: i) fusion of the articulated flight thorax (queens) into a rigid box optimized to support the muscles that operate the head, legs and abdomen, ii) redesign of internal cuticular structures for better bracing and muscle attachment, iii) substantial enlargement of the neck muscles for suspending and moving the head, iv) lengthening of the external trochanter muscles, predominant for the leg actions that lift the body off the ground, v) modified angle of the petiole muscles that are key for flexion of the abdomen. We measured volumes and pennation angles for a few key muscles to assess their increased efficacy. Our comparisons of additional workers across five genera in subfamilies Dorylinae and Myrmicinae show these modifications in the wingless thorax to be consistent. In contrast, a mutillid wasp showed a different pattern of muscle adaptations as a result of the lack of wing muscles. Conclusions Rather than simply a subtraction of costly flight muscles, we propose the ant worker thorax evolved into a power core underlying stronger mandibles, legs, and sting. This contrasts with solitary flightless insects where the lack of central place foraging generated distinct selective pressures for rearranging the thorax. Stronger emphasis is needed on innovations of social insects as individuals at the phenotypic level to further our understanding of the evolution of social behaviours.

Sign in / Sign up

Export Citation Format

Share Document