scholarly journals Superorganismal anisogamy: queen–male dimorphism in eusocial insects

2020 ◽  
Vol 287 (1928) ◽  
pp. 20200635
Author(s):  
Jussi Lehtonen ◽  
Heikki Helanterä

Colonies of insects such as ants and honeybees are commonly viewed as ‘superorganisms’, with division of labour between reproductive ‘germline-like’ queens and males and ‘somatic’ workers. On this view, properties of the superorganismal colony are comparable with those of solitary organisms to such an extent that the colony itself can be viewed as a unit analogous to an organism. Thus, the concept of a superorganism can be useful as a guide to thinking about life history and allocation traits of colonies as a whole. A pattern that seems to reoccur in insects with superorganismal societies is size dimorphism between queens and males, where queens tend to be larger than males. It has been proposed that this is analogous to the phenomenon of anisogamy at the level of gametes in organisms with separate sexes; more specifically, it is suggested that this caste dimorphism may have evolved via similar selection pressures as gamete dimorphism arises in the ‘gamete competition’ theory for the evolution of anisogamy. In this analogy, queens are analogous to female gametes, males are analogous to male gametes, and colony survival is analogous to zygote survival in gamete competition theory. Here, we explore if this question can be taken beyond an analogy, and whether a mathematical model at the superorganism level, analogous to gamete competition at the organism level, may explain the caste dimorphism seen in superorganismal insects. We find that the central theoretical idea holds, but that there are also significant differences between the way this generalized ‘propagule competition’ theory operates at the levels of solitary organisms and superorganisms. In particular, we find that the theory can explain superorganismal caste dimorphism, but compared with anisogamy evolution, a central coevolutionary link is broken, making the requirements for the theory to work less stringent than those found for the evolution of anisogamy.

2015 ◽  
Vol 282 (1811) ◽  
pp. 20150704 ◽  
Author(s):  
J. Frances Kamhi ◽  
Kelley Nunn ◽  
Simon K. A. Robson ◽  
James F. A. Traniello

Complex social structure in eusocial insects can involve worker morphological and behavioural differentiation. Neuroanatomical variation may underscore worker division of labour, but the regulatory mechanisms of size-based task specialization in polymorphic species are unknown. The Australian weaver ant, Oecophylla smaragdina , exhibits worker polyphenism: larger major workers aggressively defend arboreal territories, whereas smaller minors nurse brood. Here, we demonstrate that octopamine (OA) modulates worker size-related aggression in O. smaragdina . We found that the brains of majors had significantly higher titres of OA than those of minors and that OA was positively and specifically correlated with the frequency of aggressive responses to non-nestmates, a key component of territorial defence. Pharmacological manipulations that effectively switched OA action in major and minor worker brains reversed levels of aggression characteristic of each worker size class. Results suggest that altering OA action is sufficient to produce differences in aggression characteristic of size-related social roles. Neuromodulators therefore may generate variation in responsiveness to task-related stimuli associated with worker size differentiation and collateral behavioural specializations, a significant component of division of labour in complex social systems.


2020 ◽  
Vol 375 (1813) ◽  
pp. 20200061 ◽  
Author(s):  
Geoff A. Parker

The past half century has seen the development of the field of post-ejaculatory sexual selection, the sequel to sexual selection for mate-acquisition (pre-ejaculatory) described by Darwin. In richness and diversity of adaptations, post-ejaculatory selection rivals that of pre-ejaculatory sexual selection. Anisogamy—and hence two sexes—likely arose by primeval gamete competition, and sperm competition remains a major force maintaining high sperm numbers. The post-ejaculatory equivalent of male–male competition for matings, sperm competition was an intense ancestral form of sexual selection, typically weakening as mobility and internal fertilization developed in many taxa, when some expenditure became diverted into pre-ejaculatory competition. Sperm competition theory has been relatively successful in explaining variation in relative testes size and sperm numbers per ejaculate and is becoming more successful in explaining variation in sperm phenotype. Sperm competition has generated many other male adaptations such as seminal fluid proteins that variously modify female reproduction towards male interests, and copulatory plugs, prolonged copulations and post-ejaculatory guarding behaviour that reduce female remating probability, many of which result in sexual conflict. This short survey of conceptual developments is intended as a broad overview, mainly as a primer for new researchers. This article is part of the theme issue ‘Fifty years of sperm competition'.


2020 ◽  
Vol 64 (4-5-6) ◽  
pp. 267-273
Author(s):  
Sruthi Unnikrishnan ◽  
Raghavendra Gadagkar

Division of labour among workers (non-reproductive division of labour), a characteristic feature of eusocial insects enables the efficient functioning of their colonies. In many advanced insect societies division of labour is based on age (age polyethism). Primitively eusocial insects however are believed to have a weak age polyethism. Here we investigated the role of age in non-reproductive division of labour in the tropical primitively eusocial wasp, Ropalidia cyathiformis and compared it with that in Ropalidia marginata, a congeneric species that exhibits relatively strong age polyethism. Age had a significant effect on the first performance of the four tasks studied; tasks were initiated in the sequence feed larva, build, bring food and bring building material. We measured task performance as the absolute frequency of tasks performed (FTP) and the probability of performing a task relative to other tasks (PTP) and age as absolute age in days since eclosion as well as relative age compared to nestmates. FTP varied significantly with both absolute and relative age, although absolute age explained more variance. PTP varied significantly with absolute age but not always with relative age. This is contrary to R. marginata, where more variation is explained by relative age than by absolute age. There was no trade-off between intranidal and extranidal tasks in R. cyathiformis unlike in R. marginata where the frequency of intranidal tasks decreased and that of extranidal tasks increased with age. We conclude that age polyethism is weak and less flexible in R. cyathiformis compared to that in R. marginata.


2021 ◽  
Author(s):  
Susanne Siegmann ◽  
Romana Feitsch ◽  
Daniel W Hart ◽  
Nigel C Bennett ◽  
Dustin J Penn ◽  
...  

It has been proposed that naked mole-rat (Heterocephalus glaber) societies resemble those of eusocial insects by showing a division of labour among non-breeding individuals. Earlier studies suggested that non-breeders belong to distinct castes that specialise permanently or temporarily on specific cooperative tasks. In contrast, recent research on naked mole-rats has shown that behavioural phenotypes are continuously distributed across non-breeders and that mole-rats exhibit considerable behavioural plasticity suggesting that individuals may not specialise permanently on work tasks. However, it is currently unclear whether individuals specialise temporarily and whether there is a sex bias in cooperative behaviour among non-breeders. Here we show that non-breeding individuals vary in overall cooperative investment, but do not specialise on specific work tasks. Within individuals, investment into specific cooperative tasks such as nest building, food carrying and burrowing are positively correlated, and there is no evidence that individuals show trade-offs between these cooperative behaviours. Non-breeding males and females do not differ in their investment in cooperative behaviours and show broadly similar age and body mass related differences in cooperative behaviours. Our results suggest that non-breeding naked mole-rats vary in their overall contribution to cooperative behaviours and that some of this variation may be explained by differences in age and body mass. Our data provide no evidence for temporary specialisation, as found among some eusocial insects, and suggests that the behavioural organisation of naked mole-rats resembles that of other cooperatively breeding vertebrates more than that of eusocial insect species.


2019 ◽  
Vol 110 (3) ◽  
pp. 388-396
Author(s):  
Ming-Chung Chiu ◽  
Wen-Jer Wu ◽  
Li-Chuan Lai

AbstractBody size is an important life-history trait in eusocial insects which plays a key role in colony fitness. The division of labour, represented by caste polyethism, correlates with divergent morphological traits. Size polymorphism has been noted in the tropical fire ant, Solenopsis geminata; however, little is known regarding the differences in the size distributions of workers performing foraging tasks. In the present study, task partitioning was observed in the foraging activities of S. geminata. Two subgroups among foraging workers of S. geminata were discovered using the Gaussian mixture model: a large worker group (head width ≥ 0.924 mm) and a small worker group (head width < 0.924 mm). The foraging worker population comprised two distinct groups – 25.64% were large workers and 74.36% were small workers. Larger workers delivered heavier seeds faster than smaller workers, but this difference became less apparent when lighter seeds were being carried. When large prey such as crickets was encountered during foraging, S. geminata partitioned their tasks into cutting and transportation. The large workers were observed to cut cricket prey into fragments with their longer mandibles, and the small workers then transported these fragments back to the nest. These results present evidence of task partitioning among tropical fire ants, with different tasks being performed by ants of different castes.


2015 ◽  
Vol 93 (8) ◽  
pp. 615-625 ◽  
Author(s):  
M.H. Richards ◽  
C. Course

Reproductive division of labour in social carpenter bees differs from that in classically eusocial insects because reproductive output and ergonomic inputs are positively correlated—dominant females monopolize both foraging and reproduction. We quantified ergonomic skew in the facultatively social bee Xylocopa virginica (L., 1771) (eastern carpenter bee) based on detailed observations of foraging activity by individually marked females in 2009. Unusually for a univoltine bee, this species exhibits a spring foraging phase during which females feed pollen to other adults, probably as part of behavioural interactions to establish dominance hierarchies. During brood-provisioning, foraging in social nests was dominated by one female at a time, with replacement by a succession of foragers as dominants disappeared and were succeeded by a subordinate. The principal foragers (individuals that did the largest share of foraging in each colony) did 85%–100% of all pollen trips, so contributions to pollen-provisioning by female nest mates were highly uneven. Individual foraging rate was unaffected by group size and total colony foraging effort was a function of the number of foragers per group. Transient females that moved to new nests were as successful in achieving dominant forager status as females resident in their natal nests. This evidence indicates that colony social organisation is based on reproductive queues, whereby the first-ranked bee is the dominant forager and subordinates queue for opportunities to replace her.


2021 ◽  
Vol 376 (1823) ◽  
pp. 20190729 ◽  
Author(s):  
Ido Pen ◽  
Thomas Flatt

Between the 1930s and 1960s, evolutionary geneticists worked out the basic principles of why organisms age. Despite much progress in the evolutionary biology of ageing since that time, however, many puzzles remain. The perhaps most fundamental of these is the question of which organisms should exhibit senescence and which should not (or which should age rapidly and which should not). The evolutionary origin of ageing from a non-senescent state has been conceptually framed, for example, in terms of the separation between germ-line and soma, the distinction between parents and their offspring, and—in unicellular organisms—the unequal distribution of cellular damage at cell division. These ideas seem to be closely related to the concept of ‘division of labour' between reproduction and somatic maintenance. Here, we review these concepts and develop a toy model to explore the importance of such asymmetries for the evolution of senescence. We apply our model to the simplest case of a multicellular system: an organism consisting of two totipotent cells. Notably, we find that in organisms which reproduce symmetrically and partition damage equally, senescence is still able to evolve, contrary to previous claims. Our results might have some bearing on understanding the origin of the germ-line–soma separation and the evolution of senescence in multicellular organisms and in colonial species consisting of multiple types of individuals, such as, for example, eusocial insects with their different castes.This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?'


Author(s):  
Hiroyuki Shimoji ◽  
Shigeto Dobata

Reproductive division of labour is a hallmark of eusocial insects. However, its stability can often be hampered by the potential for reproduction by otherwise sterile nest-mates. Dominance hierarchy has a crucial role in some species in regulating which individuals reproduce. Compared with those in vertebrates, the dominance hierarchies in eusocial insects tend to involve many more individuals, and should require additional selective forces unique to them. Here, we provide an overview of a series of studies on dominance hierarchies in eusocial insects. Although reported from diverse eusocial taxa, dominance hierarchies have been extensively studied in paper wasps and ponerine ants. Starting from molecular physiological attributes of individuals, we describe how the emergence of dominance hierarchies can be understood as a kind of self-organizing process through individual memory and local behavioural interactions. The resulting global structures can be captured by using network analyses. Lastly, we argue the adaptive significance of dominance hierarchies from the standpoint of sterile subordinates. Kin selection, underpinned by relatedness between nest-mates, is key to the subordinates' acceptance of their positions in the hierarchies. This article is part of the theme issue ‘The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies’.


2018 ◽  
Vol 285 (1884) ◽  
pp. 20180975 ◽  
Author(s):  
Alberto J. C. Micheletti ◽  
Graeme D. Ruxton ◽  
Andy Gardner

Interest in the evolutionary origins and drivers of warfare in ancient and contemporary small-scale human societies has greatly increased in the last decade, and has been particularly spurred by exciting archaeological discoveries that suggest our ancestors led more violent lives than previously documented. However, the striking observation that warfare is an almost-exclusively male activity remains unexplained. Three general hypotheses have been proposed, concerning greater male effectiveness in warfare, lower male costs, and patrilocality. But while each of these factors might explain why warfare is more common in men, they do not convincingly explain why women almost never participate. Here, we develop a mathematical model to formally assess these hypotheses. Surprisingly, we find that exclusively male warfare may evolve even in the absence of any such sex differences, though sex biases in these parameters can make this evolutionary outcome more likely. The qualitative observation that participation in warfare is almost exclusive to one sex is ultimately explained by the fundamentally sex-specific nature of Darwinian competition—in fitness terms, men compete with men and women with women. These results reveal a potentially key role for ancestral conditions in shaping our species' patterns of sexual division of labour and violence-related adaptations and behavioural disorders.


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