Spider mite mothers adjust reproduction and sons' alternative reproductive tactics to immigrating alien conspecifics

Abstract

Maternal effects on environmentally induced alternative reproductive tactics (ARTs) are poorly understood but likely to be selected for if mothers can reliably predict offspring environments. We assessed maternal effects in two populations (Y and G) of herbivorous arrhenotokous spider mites Tetranychus urticae, where males conditionally express fighting and sneaking tactics in male–male combat and pre-copulatory guarding behaviour. We hypothesized that resident mothers should adjust their reproduction and sons’ ARTs to immigrating alien conspecifics in dependence of alien conspecifics posing a fitness threat or advantage. To induce maternal effects, females were exposed to own or alien socio-environments and mated to own or alien males. Across maternal and sons' reproductive traits, the maternal socio-environment induced stronger effects than the maternal mate, and G-mothers responded more strongly to Y-influence than vice versa. G-socio-environments and Y-mates enhanced maternal egg production in both populations. Maternal exposure to G-socio-environments demoted, yet maternal Y-mates promoted, guarding occurrence and timing by sons. Sneakers guarded earlier than fighters in Y-environments, whereas the opposite happened in G-environments. The endosymbiont Cardinium, present in G, did not exert any classical effect but may have played a role via the shared plant. Our study highlights interpopulation variation in immediate and anticipatory maternal responses to immigrants.

Cooperative Behaviors in Group-Living Spider Mites

“…has been suggested to possess kin discrimination abilities in activities such as spatial distribution (Le Goff et al, 2009), dispersal (Bitume et al, 2013), and mate choice (Schausberger and Sato, 2020). Experimental evidence suggests that Tetranychus urticae can also discriminate in site choice between grouplabeled kin individuals from their own population (following inbreeding) and individuals from other populations and/or their products/environmental modifications and choose microhabitats that are most favorable, whether created by kin or not (Le Goff et al, 2012;Schausberger et al, 2019). When joining others on the same leaf or plant, later arrivers/followers, initially, recipients (either on the same leaf or other leaves of the same plant if systemic downregulation of plant defense has occurred) will benefit from pioneering colonizers who are initially the actors.…”

“…Joining other groups and tightening the levels of aggregation enhance the chances of survival under predation risk because of attack abatement, even when the webbing is light or absent (Dittmann and Schausberger, 2017). An intriguing example of non-kin interactions comes from Schausberger et al (2019), who showed that individuals of one population heavily benefited (without any direct interactions) from microhabitat manipulation by webbing or host plant biochemistry by pioneering colonizers from another population (Y coming to G environment), whereas in the reverse sequence, later arrivers were negatively affected (G coming to Y environment). This was possibly mediated by G-but not Y-individuals harboring endosymbiotic bacteria Cardinium, indicating that endosymbiotic bacteria may influence kin/nonkin cooperation in spider mites (Schausberger et al, 2019).…”

Kin-Mediated Male Choice and Alternative Reproductive Tactics in Spider Mites

“…Tetranychus urticae (red form) used in experiments came from two allopatric populations, called Y and G, reared in the laboratory. The Y-population had been founded about 5 years before conducting the experiments by specimens obtained from Koppert B.V, NL, while the G-population had been founded about 2 years before the experiments by specimens collected on tomato plants in Iida, Nagano, Japan [18,31]. Either population was founded by 50 to 100 females and maintained at fluctuating sizes of hundreds to thousands of individuals.…”

“…Males grouped on leaf discs in the no-choice experiment were unfamiliar to each other. Since all environmental variables during rearing and experimentation, such as host plant species and quality, were exactly the same for both populations, we assume inherent population-specific labels [31].…”

“…In the choice experiment, mate preference by both Y-and G-males for G-females was aligned with achievable direct benefits. Preferential guarding of G-females by both Y-and G-males is adaptive because of higher fecundity of G-than Y-females; G-females mated to Y-or G-males produce 40 to 70% more eggs than Y-females mated to Y-or G-males [31]. In general, direct benefits are considered stronger drivers of mate choice than are indirect benefits [2,4,42,43].…”