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Sib-Mating Tolerance in Natural Populations of a Parasitoid Wasp bioRxiv preprint doi: https://doi.org/10.1101/169268; this version posted February 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Collet M, Amat I, Sauzet S, Auguste A, Fauvergue X, Mouton L and Desouhant E. 2018. Insects and incest: sib-mating tolerance in natural populations of a parasitoid wasp. bioRxiv, 169268, https://doi.org/10.1101/169268 An article reviewed and recommended by Peer Community In Evolutionary Biology: http://dx.doi.org/10.24072/pci.evolbiol.100047 bioRxiv preprint doi: https://doi.org/10.1101/169268; this version posted February 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Insects and incest: sib-mating tolerance in natural populations of a parasitoid wasp Marie Collet1*, Isabelle Amat1, Sandrine Sauzet1, Alexandra Auguste2, Xavier Fauvergue2, Laurence Mouton1, Emmanuel Desouhant1 1 Univ Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR5558, F-69622 Villeurbanne, France 2 INRA, CNRS, Université Côte d’Azur, ISA, France *Corresponding author: [email protected] This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100047) Abstract 1. Sib-matingSib-mating avoidance is a pervasive behaviour that likely evolves in species subject to inbreeding depression. Laboratory studies have provided elegant demonstrations of sib-sib- mating avoidance,avoidance, but small-scalesmall-scale bioassays often minimize the costs associated with mate fifindingnding and choice,choice, which could lead to spurious findings. 2. We used the hymenopteran parasitoid wasp VVenturiaenturia canescens as a model organism,organism, because previous laboratory studies revealed that sib-matingsib-mating led to a 25% decrease in fertile offspring, and that sib-matingsib-mating was partially avoided. 3. Our study consisted of a mate choice experiment in laboratory cages to determine if kin discrimination occurs in this species. We further performed a field study in which 86 wild-wild- caught males, 155 wild-caughtwild-caught females and their 226 daughters were genotypedgenotyped at eighteen microsatellite loci. With thesethese data,data, we reconstructedreconstructed the genotypegenotype of each female’s mate and estimatedestimated the relatedness of each mating pair.pair. 4. MateMate choice experimentsexperiments confirmed that females are capable of discriminatingdiscriminating kin.kin. Time to mating dependeddepended on the frequency of female encountersencounters with related and unrelated malesmales.. CContraryontrary to previously published results,results, however, nono sib-matingsib-mating avoidance was detected. In the field, the effective rate of sib-matingsib-mating did not differ from the probability that sibs encounter one other at random, which corroborates the absence of sib-matingsib-mating avoidanceavoidance.. We also detected a weak but significant male bias in dispersal,dispersal, which could reduce encounters between sibs.sibs. 5. Our results suggest that,that, despite kin discrimination, V.V. canescens toleratestolerates sib-matingsib-mating in the field.field. The weak male-biasedmale-biased dispersal cannot explain entirely this pattern.pattern. ThisThis raises the question as to why kin discrimination is maintained in this species. It further callscalls into question the idea that inbreeding depression occurs in most species with single-locussingle-locus complementary sex determination. Key-words:Key-words: Microsatellites; Inbreeding tolerance,tolerance, Kin recognition, Parasitic wasp,wasp, sl-CSD.sl-CSD. 1 bioRxiv preprint doi: https://doi.org/10.1101/169268; this version posted February 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Introduction lemurs living in socially structured groups avoid inbreeding. In mole rats, avoidance leads to a high When inbreeding lowers fitness-related reproductive skew in males, with a subset of males components, such as survival and fertility, natural that never reproduce (Cooney and Bennett, 2000). selection should favour behaviours preventing the In ring-tailed lemurs, inbreeding avoidance allows reproduction of genetically-related individuals, or females to save energy (i.e. invested in pregnancy mitigating harmful consequences referred to as and lactation) that would have be allocated to the inbreeding depression (Pusey and Wolf, 1996; production of inbred offspring, which suffer from Keller and Waller, 2002; Angeloni et al., 2011). depressed immune functions and have a reduced Inbreeding depression is caused by the expression life expectancy (Boulet et al., 2009; Charpentier et of deleterious recessive alleles at the homozygous al., 2008). It is, therefore, essential to quantify the state or by a loss of heterosis in inbred crosses costs and benefits of inbreeding avoidance to (Charlesworth and Charlesworth, 1987; Pusey and understand the consequences of inbreeding and Wolf, 1996). Selection on behaviours underlying the evolution of avoidance behaviours. inbreeding avoidance should thus depend on inbreeding load, which balances the advantages of Several behavioural and physiological inbreeding avoidance with the costs of strategies to avoid inbreeding risks have evolved in implementing adapted physiological or behavioural animals, including sib-mating avoidance, dispersal responses. Selection may also depend on the (Greenwood et al., 1978; Szulkin and Sheldon, benefits of inbreeding in terms of inclusive fitness, 2008), polyandry, extra-pair paternity, divorce as inbreeding results in an increased representation (Hatchwell et al., 2000; Cornell and Tregenza, 2007; of genes identical by descent in the offspring (Kokko Cohas et al., 2008; Lardy et al., 2011; Reid et al., and Ots, 2006; Puurtinen, 2011; Duthie and Reid, 2015; Duthie and Reid, 2016), and postcopulatory 2016). mechanisms, such as the preferential use of sperm from unrelated males by inseminated females Responses to inbreeding risk reflect the (Tregenza and Wedell, 2002; Bretman et al., 2004). benefits and costs associated with inbreeding and Mate choice is probably the most pervasive inbreeding avoidance. Observations range from behaviour for sib-mating avoidance (Pusey and systematic inbreeding avoidance to inbreeding Wolf, 1996) and relies mostly on sib recognition tolerance or even inbreeding preference (Szulkin et mediated by chemical communication (Howard and al., 2013). For example, inbreeding preference was Blomquist, 2005; Johansson and Jones, 2007; observed in the cichlid fish Pelvicachromis Charpentier et al., 2008a; Bonadonna and Sanz- taeniatus, where inbreeding does not the lower Aguilar, 2012). It is nonetheless important to note survival and growth rate of young (Thünken et al., that kin recognition mechanisms can arise from 2007). Related pairs further invest more in parental selective forces other than inbreeding avoidance, care and cooperate better. In rodents, such as such as nest-mate recognition, parental care, Marmota flavipentris, inbreeding is preferred territory defence, and dominance hierarchies despite lower survival of inbred progeny. This among others (Mateo, 2004). The balance between preference can be explained by the large variation the costs and benefits associated with inbreeding of male reproductive success and the composition avoidance also depend on environmental factors, of social groups, where males mating with related such as population density, spatial or social females do not suffer decreased annual population structure. A low population density reproductive success compared to the majority of constrains mate availability and encounter rates males with little or no reproductive success (Olson and may, therefore, influence mate choice (Kokko et al., 2012). In contrast, mole rats or ring-tailed and Rankin, 2006; Duthie and Reid, 2016). In the 2 bioRxiv preprint doi: https://doi.org/10.1101/169268; this version posted February 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. lizard Zootoca vivipara, for example, female a social species of termite, Neotermes chilensis, choosiness is reduced when mate encounter rates dispersal of colony founding individuals is the main decrease (Breedveld and Fitze, 2015). Moreover, in mechanism to avoid inbreeding (Aguilera-Olivares the marsupial carnivore, Antechinus agilis, habitat et al., 2015). In contrast, absence of inbreeding selectivity following natal dispersal is negatively avoidance has also been documented in insects, correlated with the abundance and relatedness of including parasitoid wasps (Bourdais and Hance, females occupying the novel habitat suggesting a 2009) and Drosophila melanogaster (Tan et al., pervasive effect of inbreeding risk on dispersal 2012). The diversity of strategies unveiled in (Banks
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