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Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects

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Proceedings of the Royal Society B
Authors:
Rufus A Johnstone at University of Cambridge
Rufus A Johnstone
Michael Cant at University of Exeter
Michael Cant
Jeremy Field
Jeremy Field
Jeremy Field
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Abstract

In his famous haplodiploidy hypothesis, W. D. Hamilton proposed that high sister-sister relatedness facilitates the evolution of kin-selected reproductive altruism among Hymenopteran females. Subsequent analyses, however, suggested that haplodiploidy cannot promote altruism unless altruists capitalize on relatedness asymmetries by helping to raise offspring whose sex ratio is more female-biased than the population at large. Here, we show that haplodiploidy is in fact more favourable than is diploidy to the evolution of reproductive altruism on the part of females, provided only that dispersal is male-biased (no sex-ratio bias or active kin discrimination is required). The effect is strong, and applies to the evolution both of sterile female helpers and of helping among breeding females. Moreover, a review of existing data suggests that female philopatry and non-local mating are widespread among nest-building Hymenoptera. We thus conclude that Hamilton was correct in his claim that 'family relationships in the Hymenoptera are potentially very favourable to the evolution of reproductive altruism'.
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Sex-biased dispersal, haplodiploidy and the
evolution of helping in social insects
Rufus A. Johnstone1,*, Michael A. Cant2and Jeremy Field3
1
Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK
2
Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Penryn TR10 9EZ, UK
3
School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK
In his famous haplodiploidy hypothesis, W. D. Hamilton proposed that high sister–sister relatedness
facilitates the evolution of kin-selected reproductive altruism among Hymenopteran females. Subsequent
analyses, however, suggested that haplodiploidy cannot promote altruism unless altruists capitalize on
relatedness asymmetries by helping to raise offspring whose sex ratio is more female-biased than the
population at large. Here, we show that haplodiploidy is in fact more favourable than is diploidy to the
evolution of reproductive altruism on the part of females, provided only that dispersal is male-biased
(no sex-ratio bias or active kin discrimination is required). The effect is strong, and applies to the evol-
ution both of sterile female helpers and of helping among breeding females. Moreover, a review of
existing data suggests that female philopatry and non-local mating are widespread among nest-building
Hymenoptera. We thus conclude that Hamilton was correct in his claim that ‘family relationships in
the Hymenoptera are potentially very favourable to the evolution of reproductive altruism’.
Keywords: kin selection; local competition; cooperation; altruism; social insects
1. INTRODUCTION
Bees, wasps and ants (Hymenoptera) have haplodiploid
sex determination, whereby males arise from unfertilized
eggs and are haploid, whereas females arise from fertilized
eggs and are diploid. One consequence of haplodiploidy
is that females are more closely related to sisters (r¼
0.75) than is the case in diploids (r¼0.5). W. D. Hamilton
suggested that this difference might help to explain the
large number of origins of sociality and reproductive
altruism among females in the Hymenoptera [1]. More
recent work, both theoretical and empirical, cast doubt
on this theory. Genetic models suggest that because a
female’s relatedness to her brothers is lower under haplo-
diploidy (r¼0.25) than under diploidy (r¼0.5),
haplodiploidy can promote altruism only if altruists help
to produce young among whom females are more
common than in the general population [2]; although
there are conditions under which this may occur, it is
questionable how often they are met [3]. In addition,
empirical studies have shown that active kin discrimi-
nation is rare in the social Hymenoptera [4]. Such
findings have led to a shift in focus from genetic to eco-
logical factors favouring hymenopteran eusociality [5],
although the two are not necessarily mutually exclusive.
Here, we show that haplodiploidy is in fact favourable
to the evolution of reproductive altruism on the part of
females, provided only that dispersal is male-biased—it
is not necessary to invoke sex-ratio bias or active kin dis-
crimination. Several previous analyses of altruism in
viscous populations (with limited dispersal) have con-
sidered the impact of haplodiploidy, but none have
explored the interaction between haplodiploidy and sex-
biased dispersal as we do. In his seminal model of local
helping, Taylor [6] explicitly showed that haplodiploidy
does not alter the conditions for the evolution of helping
among adult breeders, given the assumption that males
mate on their natal patch and females then disperse (car-
rying their partner’s genes with them—effectively
ensuring identical dispersal rates for both sexes); Queller
[7] subsequently suggested that sex-biased dispersal
might alter this conclusion, but did not formally analyse
this possibility. More recently, Johnstone & Cant [8]
showed that sex-biased dispersal can favour helping
among adult breeders, but considered only the diploid
case. Lastly, Lehmann et al.[9] showed that population
viscosity can favour the evolution of sterile workers (as
opposed to helping among breeders). They explicitly
demonstrate, as Taylor [6] did, that haplodiploidy does
not affect the conclusions of their model when dispersal
is identical for both sexes (and both males and females
become workers). Unlike Taylor [6], they also briefly con-
sider the impact of sex differences in dispersal, but do not
explore in detail the interaction between sex-biased
dispersal and haplodiploidy.
Below, we build on the analyses of Lehmann et al.[9]
and Johnstone & Cant [8] to show that when dispersal
is male-biased, haplodiploidy does favour female repro-
ductive altruism, whether this takes the form of the
evolution of sterile female workers or of helping among
reproductive females. Since both analyses make very
similar assumptions about population structure, we treat
them as variants of a single model, distinguished chiefly
by their focus on the evolution of sterile female helpers or
of helping among adult reproductive females, respectively.
2. MODEL
We focus on an infinite, sexually reproducing population
divided into discrete groups or colonies, each comprising
nbreeding females or queens, possibly assisted by a
*Author for correspondence (raj1003@hermes.cam.ac.uk).
Proc. R. Soc. B (2012) 279, 787–793
doi:10.1098/rspb.2011.1257
Published online 27 July 2011
Received 15 June 2011
Accepted 5 July 2011 787 This journal is q2011 The Royal Society
... For both juvenile and adult females, and for haploidy, diploidy, haplodiploidy (arrhenotoky), and PGE, we find that the potential for altruism is given by A t =1/n, where n is the number of male and female breeders on the patch, that is, the size of the demographic "bottleneck" that generates nonzero relatedness. That is, we recover the cancellation result as it pertains to female-only altruism under haploidy, diploidy, and haplodiploidy (Taylor 1992a;Johnstone and Cant 2008;Gardner 2010;Johnstone et al. 2012), and show that it also extends to female-only altruism under male PGE (Fig. 1a,d). ...
... More generally, these results may be linked to the extreme sexual dimorphism observed in some of these groups (Gray 1954;Damon 2000;Palacios-Vargas and Castaño-Meneses 2009). Such sexual dimorphism may, in turn, also modulate conditions for social behaviors to evolve (e.g., sex-biased dispersal; Johnstone and Cant 2008;Gardner 2010;Johnstone et al. 2012;Supporting Information S6), and thus further modeling is needed to understand how these factors may coevolve with one another. For example, if in PGE species males evolve to be less competitive with their siblings than are females, or provide a defensive role for the nest, then this may shape the sex-allocation decisions of parents. ...
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Population stieveness has lang been thocht tae forder the evolution o altruism. Hooivver, in the maist straucht‐forrit o scenarios, the potential fur altruism is invariant wi respeck tae skail ‐ a stamagasterin ootcome that hauds fur haploidy, diploidy, and haplodiploidy (arrhenotoky). Here we pit forrit a kin‐walin model fur tae airt‐oot hoo population stieveness affects the potential fur altruism in species wi male paternal genome drap‐oot (PGD), takkin tent o altruism enactit by baith females and males, forby baith young‐anes and aulder‐anes. We find that: 1) PGD forders altruistic ongauns relative tae the ither inheritance seestems, forby tae a degree that depends on the extent o paternal genome kythin. 2) Unner PGD, skail maks mair muckle the potential fur altruism amang young‐anes and gars it less likely amang aulder‐anes. 3) The genetics o PGD can lead tae kenspeckle differences in sex‐specific potentials fur altruism, even wioot onie sex‐differences in ecology. This article is protected by copyright. All rights reserved
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... Some of the studies listed in Table 1 have suggested that haplodiploidy may have contributed to the evolution of eusociality, but not solely through relatedness as Hamilton (1964) proposed. Instead, haplodiploidy may have contributed to the origin of eusociality through other mechanisms, such as through monogamy and haplodiploidy synergistically promoting altruistic genotypes in a colony (Fromhage and Kokko, 2011), through female philopatry in haplodiploid lineages combined with male-based dispersal promoting altruistic behavior (Johnstone et al., 2012), and the ease of sex-ratio adjustment due to female-biased helping . Other potentially relevant factors linking haplodiploidy and eusociality include lifetime monogamy, sex ratio bias, and overwintering (Quiñones and Pen, 2017), and population growth rate, effective population sex ratio, and a lowered cost of altruism (Rautiala et al., 2019). ...
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... Several hypotheses have been proposed for how haplodiploidy may nevertheless have favored the origin of eusociality, as opposed to acting after eusociality was established such as through worker reproduction or worker manipulation of sex ratios (e.g., Crozier 1977;Alpedrinha et al. 2013;Alpedrinha et al. 2014;Rautiala et al. 2019). These may be divided into two types: mechanisms that produce different sex ratios among broods or nests in noneusocial species ("split sex ratios") (Seger 1983;Grafen 1986;Gardner et al. 2012) and mechanisms that concentrate closely related females within a nest (Reeve 1993;Fromhage and Kokko 2011;Johnstone et al. 2012). Mechanisms causing split sex ratios do not appear to have been common enough to have influenced the origin of eusociality (Gardner et al. 2012;Alpedrinha et al. 2013), and mechanisms causing the concentration of close relatives do not appear to have been fully developed or tested. ...
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... We have also shown that while the potential for harm is constant across the nuclear genes under sex-neutral demography, population viscosity in concert with sex-biased demography generates differences in how male harm loci evolve on autosomes and sex chromosomes. This shares conceptual similarities with how the potential for altruistic behaviour remains invariant across diploidy and haplodiploidy under sex-neutral dispersal but diverges under sex-biased dispersal [41,51,79]. This yields predictions about where male harm loci should be enriched across the genome, and how such patterns will depend on both the extent and direction of sex biases in demography. ...
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Article
  • Nov 2004
Human impact on boreal forests has been extensive during a fairly short evolutionary time scale. Character species of boreal forests, such as Formica ants, may face loss of genetic diversity, increasing inbreeding, and decreasing gene flow among extant habitat fragments owing to habitat loss and fragmentation. Here we review the genetic data on old-world boreal species of the genus Formica. In Formica ants colonies can have one or several queens (mono- and polygyny respectively) and this trait is often assumed to be linked with dispersal propensity, such that monogyne species disperse well and polygyne species disperse less well. Our analysis of the available data reveals three important aspects of the social and dispersal biology of Formica. First, the traditional division in mono- and polygyne species is too simple and we propose a population-based division into highly polygyne, weakly or moderately polygyne, and monogyne populations. Second, there is indeed an association between colony kin structure and dispersal in the predicted direction, i.e. restricted dispersal in polygyne species. However, this only holds for between-population differentiation, not within population genetic viscosity. When genetic viscosity within populations was examined most species nevertheless showed a negative relationship between F1s and relatedness, indicating that low relatedness (many queens) is associated with reduced dispersal also locally. Only one species (F. exsecta) showed a significant positive relationship. Finally, we predict that sex-biased dispersal may be a common trait in Formica species, although data on more species are needed to confirm this.
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Nuclear and mitochondrial genetic structure in two social forms of the fire ant Solenopsis invicta: Insights into transitions to an alternate social organization
Article
  • Jun 1997
  • HEREDITY
We describe genetic structure at microgeographical scales in two social forms of the introduced fire ant Solenopsis invicta using nuclear and mitochondrial markers. Fire ant populations in northern Georgia, U.S.A. are structured in fundamentally different ways at the two genomes. Virtually all nuclear genetic variation resides within sampling sites; no differentiation was apparent between the social forms and only minimal differentiation was found among sites in only one social form (the polygyne form, which has nests with numerous queens). In contrast, substantial mtDNA variation exists at all levels; the forms are significantly differentiated and strong divergence was detected among sites in the polygyne form. No mtDNA differentiation was found among sites in the monogyne form (which has nests with a single queen). These results are predicted on the basis of the social biology of the ants. Monogyne queens and males of both forms presumably disperse widely, and polygyne queens commonly mate with monogyne males, thus explaining the uniformity of nuclear allele frequencies across sampling sites and between the forms. Polygyne queens display habits consistent with limited dispersal, and queens of both forms seem unable to establish themselves as reproductives in nests of the alternate form, thus explaining the strong microgeographical structure within the polygyne form and differentiation between the forms found using mtDNA markers. The mtDNA haplotypes are distributed among sites in a manner that suggests a mechanism for the spread of polygyny in introduced fire ants. Monogyne queens apparently mate occasionally with polygyne males and acquire a Mendelian nuclear factor allowing the expression of polygyny in their sexual daughters.Keywords: allozymes, fire ants, genetic structure, mtDNA, social organization, Solenopsis invicta
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