scholarly journals The weird eusociality of polyembryonic parasites

2021 ◽  
Vol 17 (4) ◽  
Author(s):  
Brian A. Whyte

Some parasitoid wasps possess soldier castes during their parasitic larval stage, but are often neglected from our evolutionary theories explaining caste systems in animal societies. This is primarily due to the polyembryonic origin of their societies. However, recent discoveries of polyembryonic trematodes (i.e. flatworms) possessing soldier castes require us to reconsider this reasoning. I argue we can benefit from including these polyembryonic parasites in eusocial discussions, for polyembryony and parasitism are taxonomically vast and influence the evolution of social behaviours and caste systems in various circumstances. Despite their polyembryony, their social evolution can be explained by theories of eusociality designed for parent–offspring groups, which are the subjects of most social evolution research. Including polyembryonic parasites in these theories follows the trend of major evolutionary transitions theory expanding social evolution research into all levels of biological organization. In addition, these continued discoveries of caste systems in parasites suggest social evolution may be more relevant to parasitology than currently acknowledged.

2014 ◽  
Vol 369 (1642) ◽  
pp. 20130365 ◽  
Author(s):  
Helen C. Leggett ◽  
Sam P. Brown ◽  
Sarah E. Reece

One of the most striking facts about parasites and microbial pathogens that has emerged in the fields of social evolution and disease ecology in the past few decades is that these simple organisms have complex social lives, indulging in a variety of cooperative, communicative and coordinated behaviours. These organisms have provided elegant experimental tests of the importance of relatedness, kin discrimination, cooperation and competition, in driving the evolution of social strategies. Here, we briefly review the social behaviours of parasites and microbial pathogens, including their contributions to virulence, and outline how inclusive fitness theory has helped to explain their evolution. We then take a mechanistically inspired ‘bottom-up’ approach, discussing how key aspects of the ways in which parasites and pathogens exploit hosts, namely public goods, mobile elements, phenotypic plasticity, spatial structure and multi-species interactions, contribute to the emergent properties of virulence and transmission. We argue that unravelling the complexities of within-host ecology is interesting in its own right, and also needs to be better incorporated into theoretical evolution studies if social behaviours are to be understood and used to control the spread and severity of infectious diseases.


2018 ◽  
pp. 151-178
Author(s):  
Richard R. Strathmann

Modes of development of marine crustaceans and other marine invertebrates include presence or absence of a larval stage, of larval feeding, and of maternal protection of offspring. These different developmental modes impose different compromises (trade-offs) between the number of offspring and their size or the extent of maternal protection. Crustaceans differ from many marine animals in not shedding eggs prior to fertilization, which eliminates the complication of selection on size of eggs as a target for sperm. Features shared with marine invertebrates of several phyla include rare and ancient origins of feeding larvae, irreversible losses of a feeding larval stage, a constraint on brooding imposed by embryos’ need for oxygen, and possible benefits from slower development of protected embryos. Crustaceans differ, however, in having a diverse exoskeletal tool kit that has provided unusual capabilities. Nauplii and zoeae are diverse in form, behavior, and habitat, despite each being nominally one type of larva. Nauplii, as feeding larvae, have adapted to both the benthos and plankton. Settling stages (cyprids and decapodids) with enhanced speed have evolved twice. Some very large adults can supply their large broods with oxygen. Capacity for defense of offspring and home has led a few times to eusociality. The need to molt to grow and change form imposes episodic risk and growth and, in some cases, links evolution of egg size and size at metamorphosis. Crustaceans’ diverse life histories enable comparisons with broad implications for marine invertebrates: opportunity for dispersal is similar for larvae and adults of some crustaceans, demonstrating that marine larvae need not be adaptations for dispersal; development from very small eggs is enabled by less equipment needed for first larval feeding and also by postlarval stages being parasites; eggs shed into the water suffer greater mortality than planktonic larvae or brooded eggs, yet some planktonic crustaceans depend on benthic resting eggs for persistence of populations; larvae escape predation in diverse ways, and bigger larvae are not consistently safer; predation near the seafloor makes settlement a risky stage. Parallels with other taxa are numerous, but the crustacean exoskeletal tool kit has conferred unusual evolutionary opportunities and constraints. Even among marine crustaceans, however, evolutionary options for life histories differ among clades because of rare evolutionary origins of traits of larvae and mothers and biased evolutionary transitions in those traits.


2016 ◽  
Vol 371 (1701) ◽  
pp. 20150442 ◽  
Author(s):  
Eugene V. Koonin

The history of life is punctuated by evolutionary transitions which engender emergence of new levels of biological organization that involves selection acting at increasingly complex ensembles of biological entities. Major evolutionary transitions include the origin of prokaryotic and then eukaryotic cells, multicellular organisms and eusocial animals. All or nearly all cellular life forms are hosts to diverse selfish genetic elements with various levels of autonomy including plasmids, transposons and viruses. I present evidence that, at least up to and including the origin of multicellularity, evolutionary transitions are driven by the coevolution of hosts with these genetic parasites along with sharing of ‘public goods’. Selfish elements drive evolutionary transitions at two distinct levels. First, mathematical modelling of evolutionary processes, such as evolution of primitive replicator populations or unicellular organisms, indicates that only increasing organizational complexity, e.g. emergence of multicellular aggregates, can prevent the collapse of the host–parasite system under the pressure of parasites. Second, comparative genomic analysis reveals numerous cases of recruitment of genes with essential functions in cellular life forms, including those that enable evolutionary transitions. This article is part of the themed issue ‘The major synthetic evolutionary transitions’.


Behaviour ◽  
2021 ◽  
pp. 1-20
Author(s):  
Adam R. Reddon ◽  
Tommaso Ruberto ◽  
Simon M. Reader

Abstract Aggression is costly, and animals have evolved tactics to mitigate these costs. Submission signals are an underappreciated example of such adaptations. Here we review submissive behaviour, with an emphasis on non-primates. We highlight the design of submission signals and how such signals can reduce costs. Animal societies necessitate frequent social interactions, which can increase the probability of conflict. Where maintaining group proximity is essential, animals cannot avoid aggression by fleeing. Mutual interest between group members may also select for efficient conflict avoidance and resolution mechanisms. As a result, submission signals may be especially well developed among group living species, helping social animals to overcome potential costs of recurring conflict that could otherwise counter the benefits of group living. Therefore, submission signalling can be a crucial aspect of social living and is deserving of specific attention within the broader context of social evolution and communication.


2020 ◽  
Vol 7 (7) ◽  
pp. 200517
Author(s):  
Karen M. Kapheim ◽  
Beryl M. Jones ◽  
Eirik Søvik ◽  
Eckart Stolle ◽  
Robert M. Waterhouse ◽  
...  

Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific changes in gene expression, but the key nodes that drive these regulatory changes are unknown. We examined the relationship between social organization and lineage-specific microRNAs (miRNAs). Genome scans across 12 bee species showed that miRNA copy-number is mostly conserved and not associated with sociality. However, deep sequencing of small RNAs in six bee species revealed a substantial proportion (20–35%) of detected miRNAs had lineage-specific expression in the brain, 24–72% of which did not have homologues in other species. Lineage-specific miRNAs disproportionately target lineage-specific genes, and have lower expression levels than shared miRNAs. The predicted targets of lineage-specific miRNAs are not enriched for genes with caste-biased expression or genes under positive selection in social species. Together, these results suggest that novel miRNAs may coevolve with novel genes, and thus contribute to lineage-specific patterns of evolution in bees, but do not appear to have significant influence on social evolution. Our analyses also support the hypothesis that many new miRNAs are purged by selection due to deleterious effects on mRNA targets, and suggest genome structure is not as influential in regulating bee miRNA evolution as has been shown for mammalian miRNAs.


1999 ◽  
Vol 354 (1388) ◽  
pp. 1395-1405 ◽  
Author(s):  
Ana B. Sendova-Franks ◽  
Nigel R. Franks

The prospect of generic principles of biological organization being uncovered through the increasingly broad use of the concepts of ‘self–assembly’ and ‘self–organization’ in biology will only be fulfilled if students of different levels of biological organization use the same terms with the same meanings. We consider the different ways the terms ‘self–assembly’ and ‘self–organization’ have been used, from studies of molecules to studies of animal societies. By linking ‘self–assembly’ and ‘self–organization’ with division of labour, we not only put forward a distinction between the underlying concepts but we are also able to relate them to the question: Why has a certain structure been favoured by natural selection? Using the particularly instructive case of social resilience in ant colonies, we demonstrate that the principle of self–organizing self–assembly may apply to higher levels of biological organization than previously considered. We predict that at the level of interactions among organisms within the most advanced animal societies, specialization through learning has a crucial role to play in re–assembly processes. This review may also help important commonalities and differences to be recognized between ordering mechanisms up to the social level and those further up the biological hierarchy, at the level of ecological communities.


2013 ◽  
Vol 9 (6) ◽  
pp. 20130454 ◽  
Author(s):  
Stephanie J. Kamel ◽  
Richard K. Grosberg

Until recently, little attention has been paid to the existence of kin structure in the sea, despite the fact that many marine organisms are sessile or sedentary. This lack of attention to kin structure, and its impacts on social evolution, historically stems from the pervasive assumption that the dispersal of gametes and larvae is almost always sufficient to prevent any persistent associations of closely related offspring or adults. However, growing evidence, both theoretical and empirical, casts doubt on the generality of this assumption, not only in species with limited dispersal, but also in species with long dispersive phases. Moreover, many marine organisms either internally brood their progeny or package them in nurseries, both of which provide ample opportunities for kinship to influence the nature and outcomes of social interactions among family members. As the evidence for kin structure within marine populations mounts, it follows that kin selection may play a far greater role in the evolution of both behaviours and life histories of marine organisms than is presently appreciated.


2018 ◽  
Vol 16 (2) ◽  
pp. 147470491875699
Author(s):  
Omar Tonsi Eldakar ◽  
J. Oliver Kammeyer ◽  
Nikhil Nagabandi ◽  
Andrew C. Gallup

Altruism presents an evolutionary paradox, as altruistic individuals are good for the group yet vulnerable to exploitation by selfish individuals. One mechanism that can effectively curtail selfishness within groups is punishment. Here, we show in an evolutionary game-theoretical model that punishment can effectively evolve and maintain high levels of altruism in the population, yet not all punishment strategies were equally virtuous. Unlike typical models of social evolution, we explicitly altered the extent to which individuals vary in their power over others, such that powerful individuals can more readily punish and escape the punishment of others. Two primary findings emerged. Under large power asymmetries, a powerful selfish minority maintained altruism of the masses. In contrast, increased symmetry of power among individuals produced a more egalitarian society held together by altruism and punishment carried out by the collective. These extremes are consistent with the coercive nature of the powerful elites in social insects and egalitarian mechanisms of punishment in humans such as coalitional enforcement and gossip. Our overall findings provide insights into the importance of oversight, the consequences to changes in the power structure of social systems, and the roots of hypocrisy and corruption in human and nonhuman animal societies.


2019 ◽  
Vol 36 (10) ◽  
pp. 2105-2110 ◽  
Author(s):  
Kirsten I Verster ◽  
Jennifer H Wisecaver ◽  
Marianthi Karageorgi ◽  
Rebecca P Duncan ◽  
Andrew D Gloss ◽  
...  

Abstract Horizontal gene transfer events have played a major role in the evolution of microbial species, but their importance in animals is less clear. Here, we report horizontal gene transfer of cytolethal distending toxin B (cdtB), prokaryotic genes encoding eukaryote-targeting DNase I toxins, into the genomes of vinegar flies (Diptera: Drosophilidae) and aphids (Hemiptera: Aphididae). We found insect-encoded cdtB genes are most closely related to orthologs from bacteriophage that infect Candidatus Hamiltonella defensa, a bacterial mutualistic symbiont of aphids that confers resistance to parasitoid wasps. In drosophilids, cdtB orthologs are highly expressed during the parasitoid-prone larval stage and encode a protein with ancestral DNase activity. We show that cdtB has been domesticated by diverse insects and hypothesize that it functions in defense against their natural enemies.


2016 ◽  
Vol 3 (6) ◽  
pp. 160178 ◽  
Author(s):  
Mary Friel ◽  
Hansjoerg P. Kunc ◽  
Kym Griffin ◽  
Lucy Asher ◽  
Lisa M. Collins

Social interactions among individuals are often mediated through acoustic signals. If acoustic signals are consistent and related to an individual's personality, these consistent individual differences in signalling may be an important driver in social interactions. However, few studies in non-human mammals have investigated the relationship between acoustic signalling and personality. Here we show that acoustic signalling rate is repeatable and strongly related to personality in a highly social mammal, the domestic pig ( Sus scrofa domestica ). Furthermore, acoustic signalling varied between environments of differing quality, with males from a poor-quality environment having a reduced vocalization rate compared with females and males from an enriched environment. Such differences may be mediated by personality with pigs from a poor-quality environment having more reactive and more extreme personality scores compared with pigs from an enriched environment. Our results add to the evidence that acoustic signalling reflects personality in a non-human mammal. Signals reflecting personalities may have far reaching consequences in shaping the evolution of social behaviours as acoustic communication forms an integral part of animal societies.


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