Inbreeding and the Evolution of Sociality in Arthropods
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Naturwissenschaften DOI 10.1007/s00114-012-0961-x REVIEW Inbreeding and the evolution of sociality in arthropods Seyed Mohammad Tabadkani & Jamasb Nozari & Mathieu Lihoreau Received: 13 May 2012 /Revised: 4 August 2012 /Accepted: 10 August 2012 # Springer-Verlag 2012 Abstract Animals have evolved strategies to optimally bal- the progeny. Inbred mating increases homozygosity in off- ance costs and benefits of inbreeding. In social species, spring and favors the expression of deleterious recessive these adaptations can have a considerable impact on the alleles, often resulting in a decline of fitness traits known structure, the organization, and the functioning of groups. as inbreeding depression (Charlesworth and Willis 2009). Here, we consider how selection for inbreeding avoidance Costs of inbreeding depression are further amplified at the fashions the social behavior of arthropods, a phylum exhib- population level as high homozygosity reduces the evolu- iting an unparalleled richness of social lifestyles. We first tionary potentials of the populations and thus increases their examine life histories and parental investment patterns de- susceptibility to fast changing environments (Cheptou and termining whether individuals should actively avoid or pre- Donohue 2011). Therefore, many animals have evolved fer inbreeding. Next, we illustrate the diversity of inbreeding strategies to prevent (or reduce) the incidence of mating avoidance mechanisms in arthropods, from the dispersal of with their kin (Pusey and Wolf 1996). Mating with too individuals to the rejection of kin during mate choice and genetically distant individuals can also reduce the fitness the production of unisexual broods by females. Then, we of the progeny and lead to an outbreeding depression, for address the particular case of haplodiploid insects. Finally, instance through the disruption of coadapted gene com- we discuss how inbreeding may drive and shape the evolu- plexes or local adaptations (Charlesworth and Willis tion of arthropods societies along two theoretical pathways. 2009). However, opportunities for extreme outbreeding are rare in nature and few animals may avoid mating with their Keywords Arthropods . Haplodiploidy . Inbreeding non-kin (Bateson 1978, 1983). avoidance . Social evolution On the other hand, inbreeding has substantial positive effects on the parent’s inclusive fitness by increasing their representation of genes identical by descent in future gen- Introduction erations (Parker 1979; Kokko and Ots 2006). For instance, a female mated with her brother has a 50 % chance to transmit Inbreeding is a primary factor defining the genetic structure not only one but two gene copies to the offspring. As the of animal groups and populations (Keller and Waller 2002). cost of inbreeding depression and the kin-selected benefit of On the one hand, inbreeding incurs important fitness costs to inbreeding do not necessarily cancel out, their balance deter- mines whether individuals should actively avoid or favor mating with their kin (Parker 1979, 2006; Lehmann and Communicated by: Sven Thatje : Perrin 2003; Kokko and Ots 2006; Puurtinen 2011). S. M. Tabadkani (*) J. Nozari Whether animals should prefer or avoid inbreeding is Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Tehran, particularly important in social species where close relatives PO Box 4111, Karaj, Iran frequently interact as inbreeding tolerance at the individual e-mail: [email protected] level potentially affects the structure and functioning of groups. Most knowledge about how social animals strike M. Lihoreau School of Biological Sciences and the Charles Perkins Centre, an optimal balance between inbreeding and outbreeding has The University of Sydney, been deduced from studies on birds and mammals (Blouin Sydney, NSW, Australia and Blouin 1988; Thornhill 1993; Pusey and Wolf 1996). Naturwissenschaften However, growing evidence on social insects (Gerloff et al. reproduction (Trivers 1972; Thornhill and Alcock 1983), the 2003), mites (Tien et al. 2011), and spiders (Bilde et al. models suggest that inbreeding tolerance should vary be- 2005) reveal the profound impact of inbreeding on the tween sexes, thus generating conflicts zones in which males fitness, the physiology, and the behavior of arthropods too. and females interests differ (Parker 1979, 2006). For in- These recent observations thus shed new lights on the role stance, when mating does not affect future mating opportu- of inbreeding in the regulation of social interactions in a nities, males should prefer mating with their sisters if phylum exhibiting an exceptionally rich spectrum of social inbreeding depression is less than two thirds, while females forms, from temporary aggregations (Costa 2006) to colo- should avoid mating with their brothers if inbreeding de- nies of thousands of individuals working together as a pression is greater than one third (Parker 1979, 2006; “superorganism” (Hölldobler and Wilson 2009). Lehmann and Perrin 2003; but see Kokko and Ots 2006; The aim of our review is to discuss the role of inbreeding Puurtinen 2011 for different values). as a major evolutionary factor driving and shaping the social Mating opportunities are also expected to influence in- biology of arthropods. First, we examine evolutionary mod- breeding tolerance levels and generate differences between els of inbreeding tolerance theory. Second, we illustrate the individuals of the same sex. As the parental investment diversity of inbreeding avoidance mechanisms across many increase, tolerance to inbreeding should decrease and be- arthropod taxa. Third, we address the particular case of come minimum when the opportunity of cost of mating is inbreeding in haplodiploid insects. Finally, we discuss how maximum, for instance if a male loses an outbred offspring a more comprehensive understanding of inbreeding regula- for every offspring gained by its sister (Parker 1979, 2006). tion strategies in arthropods might help in clarifying the In a comprehensive examination of this opportunity cost, intimate relationship between inbreeding and the evolution Kokko and Ots (2006) distinguished between simultaneous of sociality along alternate pathways. mate choice, where individuals can immediately choose between related and unrelated partners, and sequential choice, where partners are encountered once at a time. Balancing inbreeding and outbreeding Their model suggests that sequential choice should often generate much higher inbreeding tolerance than simultaneous Arthropods show a high variability in their tolerance to choice, thus raising the importance of the social environments inbreeding. In some species, individuals mate preferentially (mate encounter rate), in addition to inbreeding depression with their kin [e.g., flour beetles Tribolium castaneum strength and kin selected-benefits, in determining inbreeding (Nilsson et al. 2002)], whereas in others kin are rejected tolerance by individuals. [e.g., German cockroach Blattella germanica (Lihoreau et al. 2008) and the primitively social bee Lasioglossum zephyrum (Greenberg 1979)]. Variation is also observed Inbreeding avoidance mechanisms within species, for instance between individuals from labo- ratory and natural populations [paper wasp Polistes domi- In contrast to theoretical research, empirical literature in nulus (Liebert et al. 2010)]. Interpreting these differences is arthropods has almost exclusively focused on inbreeding often difficult, as the selection pressures on inbreeding avoidance strategies (but see Jennions et al. 2004; Bilde et tolerance are hardly measurable empirically. However, al. 2005; Peer and Taborsky 2005;Edvardssonetal.2008;De several evolutionary models have been proposed. Luca and Cocroft 2008; Thurin and Aron 2009; Robinson et Theory suggests that individuals should either avoid or al. 2012). These include precopulatory mechanisms, by which favor inbred matings in order to balance the cost of inbreed- individuals avoid mating with kin, and postcopulatory mech- ing depression and the kin-selected benefit of inbreeding anisms, whereby individuals invest differentially in reproduc- (Parker 1979, 2006; Lehmann and Perrin 2003; Kokko and tion depending on their relatedness with mating partners. Ots 2006; Puurtinen 2011). Because individuals from dif- ferent sexes, different populations, and different species face Dispersal different ecological and social environments to which they have to adapt, this balance should be flexible. Dispersal of males or females from their natal group is a Classical models predict that inbreeding tolerance should widespread strategy reducing risks of inbreeding in arthro- vary around a threshold value determined by the cost of pods, especially in eusocial Hymenoptera (ants, some bees, inbreeding (Parker 1979, 2006). Below this threshold, indi- and wasps) where individuals of one or a few genetic viduals should actively favor inbreeding, even when this lineages occupy a common nest and the probability of results in substantial reduction in offspring fitness. Above inbreeding is high (Table 1). this threshold, however, individuals should avoid inbreed- In ants, males (drones) and reproductive females (gynes) ing. Because males and females often invest differently in from several neighbor nests often emerge simultaneously Naturwissenschaften Table 1 Examples of inbreed- ing avoidance through dispersal Species Order Inbreeding avoidance Reference in arthropods mechanism(s) Bombus californicus