Parental effects of male alternative reproductive tactics (ARTs) on ARTs of haploid sons

Abstract

Alternative reproductive tactics (ARTs) represent distinct behavioural phenotypes to maximize reproductive success within the same sex, primarily males, and may be genetically and/or conditionally determined. Across animals, intragenerational determinants of conditional ARTs are relatively well understood but transgenerational (non‐genetic) effects of parental ARTs on filial ARTs are largely unknown. Here, we assessed parental effects of conditional male ARTs on sons' ARTs in arrhenotokous spider mites Tetranychus urticae. Arrhenotoky, that is, males arising from unfertilized and females from fertilized eggs, sets the stage for sexual and transgenerational conflicts between male mates and females and their sons. Male ARTs of T. urticae are dichotomous, fighting and sneaking, and apparent in male–male combat and pre‐copulatory guarding behaviour. Due to haplodiploidy, male ARTs can only exert non‐genetic effects on sons of their mates. We hypothesized that parental ART effects are likely to occur in T. urticae because maternal ART mating status (unmated, sneaker‐ or fighter‐mated) is indicative of the offspring' social environment and ART flexibility rather prevails in younger than older males. Fighter‐mated mothers produced more offspring than unmated mothers and had a more daughter‐biased offspring sex ratio than unmated and sneaker‐mated mothers. Sons of fighter‐mated mothers were more likely to guard and did so earlier than sons of unmated and sneaker‐mated mothers. Unmated and sneaker‐mated, but not fighter‐mated, mothers produced sneaker sons that were quicker to start guarding than were fighter sons. Proximately, parental ART effects on sons' ARTs were most likely mediated by differences in seminal fluids. Ultimately, observed alterations of sons' ARTs represent adaptive maternal responses to ART phenotypes rather than manipulation by male mates. Fighter‐mated mothers tuned filial ARTs to male‐competitive environments whereas unmated and sneaker‐mated mothers tuned them to benign environments. Observed alterations in reproductive traits of fighter‐mated mothers suggest adaptive manipulation by the fighter phenotype or aligned male and female interests. Overall, our study documents previously unknown transgenerational ART effects on haploid sons' ARTs. A free Plain Language Summary can be found within the Supporting Information of this article.

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

“…Assuming that guarding propensity and ART ratio reflect the intensity of competition [20], males competed more strongly for non-kin females and when competing with non-kin males. In general, intense competition should increase male mating efforts [2].…”

“…Guarding behavior is highly important for paternity success, because of first male sperm precedence [14][15][16][17], and is thus a suitable indicator of male choice. Regarding ARTs, T. urticae males may adopt fighting or sneaking tactics before and during pre-copulatory guarding behavior [18][19][20]. ARTs of T. urticae males are conditional and reversible [18,19].…”

“…ARTs of T. urticae males are conditional and reversible [18,19]. Fighters fight with other males to gain access to T-females and to defend their guarding position; sneakers do not fight but build on speed (i.e., being quick to start guarding) and crypsis towards other males (preventing them from being fought) to succeed in gaining access to T-females and keeping their guarding position [18][19][20].…”

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

“…We hypothesized that females perceiving the arrival of alien conspecifics should adjust their reproduction, transfer information about alien conspecifics to the next generation and adjust the ARTs of sons. Maternal adjustment of sons’ ARTs may be apparent in altered guarding eagerness, ART ratio and/or timing of guarding, all of which are affecting the relative reproductive success of ARTs [39]. If immigrating alien conspecifics increase the fitness of residents via genetic and/or environmental effects, we predicted unchanged or worsened within-resident performance by ARTs.…”

“…If immigrating alien conspecifics increase the fitness of residents via genetic and/or environmental effects, we predicted unchanged or worsened within-resident performance by ARTs. By contrast, if immigrating alien conspecifics are detrimental and threaten to decrease the fitness of residents via genetic, phenotypic and/or environmental effects, we predicted optimized within-resident performance by ARTs [39], to prevent or mitigate loss of their genetic, phenotypic and/or environmental advantage in the absence of alien conspecifics.…”