Ancestral Monogamy Shows Kin Selection Is Key to the Evolution of Eusociality

Published on May 30, 2008in Science47.728
· DOI :10.1126/SCIENCE.1156108
William O. H. Hughes45
Estimated H-index: 45
(University of Leeds),
Benjamin P. Oldroyd64
Estimated H-index: 64
(USYD: University of Sydney)
+ 1 AuthorsFrancis L. W. Ratnieks82
Estimated H-index: 82
(University of Sussex)
Sources
Abstract
Close relatedness has long been considered crucial to the evolution of eusociality. However, it has recently been suggested that close relatedness may be a consequence, rather than a cause, of eusociality. We tested this idea with a comparative analysis of female mating frequencies in 267 species of eusocial bees, wasps, and ants. We found that mating with a single male, which maximizes relatedness, is ancestral for all eight independent eusocial lineages that we investigated. Mating with multiple males is always derived. Furthermore, we found that high polyandry (>2 effective mates) occurs only in lineages whose workers have lost reproductive totipotency. These results provide the first evidence that monogamy was critical in the evolution of eusociality, strongly supporting the prediction of inclusive fitness theory.
📖 Papers frequently viewed together
1971
1 Author (Edward O. Wilson)
2011
197647.73Science
References23
Newest
The generation-long primacy of kin selection in explaining the evolution of advanced eusociality in social insects has been challenged in recent papers. Does this challenge succeed? I consider three questions: is kin selection still the unchallengeable explanation for the evolution of eusociality; is the male haploidy of Hymenoptera important in this explanation; and, a subsidiary question of why are there no male workers in Hymenoptera? I briefly trace the origins of kin selection back to Darwi...
Source
#1Edward O. Wilson (Harvard University)H-Index: 109
ABSTRACT The advanced colonial state of eusociality has evolved in insects as a defense of nest sites within foraging distance of persistent food sources. In the Hymenoptera, the final step in the approach to eusociality is through a suite of preadaptations comprising simultaneous provisioning, fidelity to the nest, and a preexisting propensity toward dominance behavior and the selection of tasks according to opportunity. The only genetic change needed to cross the threshold to the eusocial grad...
Source
#1Jacobus J. Boomsma (UCPH: University of Copenhagen)H-Index: 83
I redevelop the hypothesis that lifetime monogamy is a fundamental condition for the evolution of eusocial lineages with permanent non-reproductive castes, and that later elaborations — such as multiply-mated queens and multi-queen colonies — arose without the re-mating promiscuity that characterizes non-social and cooperative breeding. Sexually selected traits in eusocial lineages are therefore peculiar, and their evolution constrained. Indirect (inclusive) fitness benefits in cooperatively bre...
Source
#1Heather M. Hines (UIUC: University of Illinois at Urbana–Champaign)H-Index: 25
#2James H. Hunt (MU: University of Missouri)H-Index: 27
Last. Sydney A. Cameron (INHS: Illinois Natural History Survey)H-Index: 31
view all 5 authors...
Eusocial wasps of the family Vespidae are thought to have derived their social behavior from a common ancestor that had a rudimentary caste-containing social system. In support of this behavioral scenario, the leading phylogenetic hypothesis of Vespidae places the eusocial wasps (subfamilies Stenogastrinae, Polistinae, and Vespinae) as a derived monophyletic clade, thus implying a single origin of eusocial behavior. This perspective has shaped the investigation and interpretation of vespid socia...
Source
The evolution of eusociality, where some individuals altruistically forgo reproduction, poses a dilemma which can be solved by kin selection, i.e. by considering relatedness among cooperating individuals. Most often, such relatedness is caused by pedigree relationships between family members. However, an alternative explanation has recently emerged in an article by Wilson and Holldobler (2005). Wilson and Holldobler see the ecological benefit of group living as the principal reason for sociality...
Source
#1Seirian Sumner (ZSL: Zoological Society of London)H-Index: 26
#2Eric R. Lucas (UCL: University College London)H-Index: 13
Last. Nick J. B. Isaac (ZSL: Zoological Society of London)H-Index: 42
view all 4 authors...
Summary Kin-selection theory underlies our basic understanding of social evolution [1, 2]. Nest drifting in eusocial insects (where workers move between nests) presents a challenge to this paradigm, since a worker should remain as a helper on her natal colony, rather than visit other colonies to which she is less closely related. Here we reveal nest drifting as a strategy by which workers may maximize their indirect fitness by helping on several related nests, preferring those where the marginal...
Source
#1Seán G. Brady (National Museum of Natural History)H-Index: 35
#2Sedonia D. SipesH-Index: 7
Last. Bryan N. Danforth (Cornell University)H-Index: 59
view all 4 authors...
Eusocial organisms are characterized by cooperative brood care, generation overlap and reproductive division of labour. Traits associated with eusociality are most developed in ants, termites, paper wasps and corbiculate bees; the fossil record indicates that each of these advanced eusocial taxa evolved in the Late Cretaceous or earlier (greater than 65 Myr ago). Halictid bees also include a large and diverse number of eusocial members, but, in contrast to advanced eusocial taxa, they are charac...
Source
#1Madeleine BeekmanH-Index: 44
#2Christian PeetersH-Index: 36
Last. M. Justin O'RiainH-Index: 21
view all 3 authors...
Unequal reproduction is widespread in animal societies. Over the last decade, there have been several attempts to derive a conceptual framework that allows diverse taxa of invertebrates and vertebrates to be compared with the aim of identifying common causes underlying reproductive division of labor. Sherman et al. (1995) used reproductive skew values, derived from variation in lifetime reproductive success, to classify taxa. Crespi and Yanega (1995), on the other hand, focused on the loss of "t...
Source
In this new assessment of the empirical evidence, an alternative to the standard model is proposed: group selection is the strong binding force in eusocial evolution; individual selection, the strong dissolutive force; and kin selection (narrowly defined), either a weak binding or weak dissolutive force, according to circumstance. Close kinship may be more a consequence of eusociality than a factor promoting its origin. A point of no return to the solitary state exists, as a rule when workers be...
Source
#1Graham J. Thompson (USYD: University of Sydney)H-Index: 21
#2Benjamin P. Oldroyd (USYD: University of Sydney)H-Index: 64
We use a likelihood-based statistical test to evaluate the extent to which the available molecular data sets can be used to falsify alternative phylogenetic hypotheses describing the inter-relationship among corbiculate bee tribes. Based on the results of this test, we explore three alternative models of behavioural character state evolution and evaluate the support each model has for single-origin versus dual-origin hypotheses for ‘highly’ eusocial behaviour. We show that only one of four data ...
Source
Cited By478
Newest
#1Huiyue ZhaoH-Index: 2
#2Yanjie LiuH-Index: 2
Last. Jiandong AnH-Index: 6
view all 5 authors...
Queen-worker conflict over the reproduction of males exists in the majority of haplodiplioidy hymenpteran species such as bees, wasps, and ants, whose workers lose mating ability but can produce haploid males in colony. Bumblebee is one of the representatives of primitively eusocial insects with plastic division labor and belongs to monandrous and facultative low polyandry species that have reproductive totipotent workers, which are capable of competing with mother queen to produce haploid males...
Source
#1Michael Mikát (Charles University in Prague)H-Index: 4
#2Daniel Benda (Charles University in Prague)H-Index: 3
Last. Jakub Straka (Charles University in Prague)H-Index: 18
view all 3 authors...
Source
#1Ornela De Gasperin (UNIL: University of Lausanne)H-Index: 7
#2Pierre Blacher (UNIL: University of Lausanne)H-Index: 4
Last. Michel Chapuisat (UNIL: University of Lausanne)H-Index: 35
view all 3 authors...
Source
#1Andrew V. Suarez (UIUC: University of Illinois at Urbana–Champaign)H-Index: 56
#2Michael A. D. Goodisman (Georgia Institute of Technology)H-Index: 31
Eusociality represents an extreme form of social behavior characterized by a reproductive division of labor. Eusociality necessarily evolved through kin selection, which requires interactions among related individuals. However, many eusocial taxa also show cooperation between non-kin groups, challenging the idea that intraspecific cooperative actions should only occur among relatives. This review explores the causes and consequences of non-kin cooperation in ants. Ants display a diversity of beh...
Source
#1Arne Matthias Jungwirth (University of Veterinary Medicine Vienna)H-Index: 6
Source
#1Gerald G. Carter (OSU: Ohio State University)H-Index: 22
Source
#1Hajime Yaguchi (University of Toyama)
#2Itaru Kobayashi (University of Toyama)
Last. Christine A. Nalepa (NCSU: North Carolina State University)H-Index: 31
view all 4 authors...
Subsocial Cryptocercus cockroaches are the sister group to termites and considered to be socially monogamous. Because genetic monogamy is a suggested requirement for evolution of cooperative breeding/eusociality, particularly in hymenopterans, clarification of the mating biology of Cryptocercus would help illuminate evolutionary trends in eusocial insects. To investigate possible extra-pair paternity in C. punctulatus, microsatellite markers were used to analyse offspring parentage, the stored s...
Source
#1Prashant Waiker (UNCG: University of North Carolina at Greensboro)H-Index: 2
#2Fabiano C. Pinto de Abreu (FFCLRP: Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto)H-Index: 2
Last. Olav Rueppell (U of A: University of Alberta)H-Index: 29
view all 6 authors...
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 relat...
Source
#1Arthur Weyna (University of Montpellier)H-Index: 3
#2Jonathan Romiguier (University of Montpellier)H-Index: 18
Last. Charles Mullon (UNIL: University of Lausanne)H-Index: 10
view all 3 authors...
The success of a eusocial colony depends on two main castes: queens that reproduce and sterile workers that help them. This division of labour is vulnerable to selfish genetic elements that enforce the development of their carriers into queens. Several factors, e.g. intra-colonial relatedness, can influence the spread of such selfish elements. Here we investigate a common yet understudied ecological setting: where hybrid larvae can develop into workers. Using mathematical modelling, we show that...
Source
Source
This website uses cookies.
We use cookies to improve your online experience. By continuing to use our website we assume you agree to the placement of these cookies.
To learn more, you can find in our Privacy Policy.