Plastic female choice to optimally balance (k)in- and out-breeding in a predatory mite

Abstract

Both close inbreeding and extreme outbreeding may negatively affect direct fitness. Optimal outbreeding theory suggests that females should preferentially mate with distantly related males. (K)in breeding theory suggests that, at similar direct fitness costs of close inbreeding and extreme outbreeding, females should prefer close kin to non-kin. Empirical evidence of plastic female choice for an optimal balance between close inbreeding and extreme outbreeding remains elusive. We tested the combined predictions of optimal outbreeding and (k)in breeding theories in predatory mites Phytoseiulus persimilis from two origins, Sicily and Greece, which suffer from both close inbreeding and extreme outbreeding depression. In three separate experiments, virgin females were presented binary choices between familiar and unfamiliar brothers, and between familiar/unfamiliar brothers and distant kin or non-kin. Females of Greece but not Sicily preferred unfamiliar to familiar brothers. females of both origins preferred distant kin to unfamiliar and familiar brothers but preferred unfamiliar brothers to non-kin. Females of Sicily but not Greece preferred familiar brothers to non-kin. The suggested kin recognition mechanisms are phenotype matching and direct familiarity, with finer-tuned recognition abilities of Greece females. Overall, our experiments suggest that flexible mate choice by P. persimilis females allows optimally balancing inclusive fitness trade-offs. Both close inbreeding and extreme outbreeding may negatively affect fitness. Close inbreeding commonly decreases direct fitness, for example, by reducing survival, reproduction, competitiveness and/or stress tolerance 1-3. Outbreeding is often advantageous to close inbreeding but its benefits depend on the level of genetic distance between mates and the choice options. Extreme outbreeding may be detrimental to direct fitness for various reasons such as underdominance (i.e. heterozygote disadvantage), breaking up advantageous co-adapted gene complexes or maladaptation 4-7. Accordingly, optimal outbreeding theory 4 states that intermediate levels of genetic relatedness between mates should yield the highest fitness gains. However, an alternative theory of mate choice, (k)in breeding theory 8,9 , recognizes that inbreeding entails kin-selected indirect fitness gains 10,11 , due to allowing genetically related males to sire offspring and increased genetic relatedness of offspring, which may counterbalance or even outweigh direct fitness costs 8,9,12. Synthesis of optimal outbreeding theory 4 and (k) in breeding theory 8,9 suggests that animals should optimally balance mate choice between kin and non-kin, in dependence of the choice options and the associated benefit-cost trade-offs in direct and indirect fitness 13. Optimally balancing mate choice between kin and non-kin requires kin recognition abilities 14-16. Kin recognition is a prime mechanism allowing to either avoid or prefer inbreeding across animals; other reported mechanisms include dispersal, polyandry, delayed...

A thelytokous predatory mite is more cannibalistic towards distant kin

“…Several phytoseiids have been found to recognize kin, including the specialist predators, Phytoseiulus persimilis , and P. macropilis ( Schausberger and Croft 2001 ), and generalist predators, Amblyseius herbicolus , Gynaeseius liturivorus , Iphiseius degenerans , and Neoseiulus californicus ( Faraji et al 2000 ; Christiansen and Schausberger 2017 ; Saitoh and Choh 2018 ; Zhang and Zhang 2022 ). Prior association and phenotype matching were mostly reported in phytoseiids ( Schausberger 2005 , 2007 ; Christiansen and Schausberger 2017 ; Schausberger and Çekin 2020 ). However, the two mechanisms are not mutually exclusive.…”