Constrained sex allocation after mating in a haplodiploid thrips species depends on maternal condition

Abstract

In females of haplodiploid animals, female production requires fertilization, whereas male production does not. Therefore, haplodiploid species can display extraordinary sex ratios. Constrained sex allocation occurs when a female cannot produce daughters. This can be due to virginity but may also occur after mating due to insemination failure, selfish genetic elements or physiological constraints. Here, we investigated the mechanism underlying constrained sex allocation in Pezothrips kellyanus. In this species some mated females produce highly female‐biased broods, yet, for unknown reasons, others produce extremely male‐biased broods. Using crossing experiments controlled for maternally inherited endosymbionts we confirmed that constrained females were successfully inseminated. Furthermore, male‐biased offspring production was not paternally inherited, ruling out paternal sex ratio elements previously identified as sex ratio distorters in some parasitoid wasps. Next, we excluded mating time and paternal fitness effects (male size) on sex allocation. However, we found that constrained sex allocation only occurred in small females producing smaller eggs than large females producing larger eggs and female‐biased broods. Consequently, the bimodal sex allocation pattern correlates with maternal condition, and may have arisen (adaptively or non‐adaptively) in association with an egg size‐mediated fertilization mechanism recently detected in some haplodiploids, with egg size positively affecting fertilization success.

Endosymbionts moderate constrained sex allocation in a haplodiploid thrips species in a temperature-sensitive way

“…Offspring sex ratio of each individual female was calculated as the percentage of male offspring in the brood. Consistent with a previous study (Katlav et al 2021a ), females showed a bimodal sex ratio pattern and were thus grouped into two categories depending on the percentage of male offspring: constrained females with 85–100% male offspring (M broods) and unconstrained females with 0–15% male offspring (F broods). Due to the bimodal nature of sex allocation in this species, a mixed effects logistic regression was used to analyse the effect of “infection status” and “temperature” (as two binary fixed factors; infected vs. uninfected; 20 vs. 25 °C) on the probability of constrained sex allocation.…”

“…We further hypothesize that the increased male production at the higher temperature may be due to an increase in constrained sex allocation. We have previously found that constrained sex allocation in P. kellyanus is linked with lower fertilization rates (Katlav et al 2021a ). Therefore, increased constrained sex allocation may prevent the expression of CI (which is only ever manifested in fertilized embryos of haplodiploid hosts).…”

“…Once mating had started with one male, the copulation activity of individual pairs was monitored to ensure that mating was not disrupted. Then each individual pair was transferred onto one lemon fruit in a small round plastic container (Nguyen et al 2017 ; Katlav et al 2021a ) and ad libitum Typha sp. pollen was added and replenished every second day.…”

“…Thrips (Thysanoptera) have evolved haplodiploidy independently from Hymenoptera and other haplodiploid lineages such as wasps (Hymenoptera), scales and whiteflies (Hemiptera), and mites (Acariformes) (Evans et al 2004 ; Nguyen et al 2015 ). As with all haplodiploids, their maternal ability of sex ratio adjustment via fertilization control in response to biotic and abiotic conditions make thrips important model organisms for testing the generality of sex allocation theories in haplodiploids (Crespi 1992 ; 1993 ; Katlav et al 2021a ). In this study, we examined the effect of bacterial endosymbionts on the sex allocation in Pezothrips kellyanus (Thripidae), a native Australian haplodiploid thrips species which is naturally infected with one Cardinium strain and one Wolbachia supergroup B strain (Nguyen et al 2016 ).…”

“…Based on comprehensive crossing experiments between infected and uninfected individuals, with analyses of egg hatch and survival to adulthood, it was found that both bacterial endosymbionts independently induce CI, with their coinfection resulting in FM-CI; however, other reproductive manipulations such as male killing and feminization were excluded (Nguyen et al 2017 ). Interestingly, females of P. kellyanus display condition-dependent constrained sex allocation which leads to split sex ratios among mated females, i.e., small mated females, despite successful insemination, produce extremely male-biased broods, whereas large mated females produce extremely female-biased broods (Katlav et al 2021a ), possibly to mitigate the costs of constrained sex allocation at the population level (Godfray 1990 ). However, it remains unknown whether the two maternally inherited endosymbionts can affect this split sex ratio pattern and/or whether the split sex ratio pattern is temperature-dependent.…”