Opposing effects of mortality factors on progeny operational sex ratio may thwart adaptive manipulation of primary sex ratio.

Gaétan Moreau,Benoit Morin,Dan T Quiring,Eldon S Eveleigh,Christopher J Lucarotti

doi:10.1002/ece3.3071

Gaétan Moreau, Benoit Morin + Show 3 more

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https://doi.org/10.1002/ece3.3071

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Abstract

Despite extensive research on mechanisms generating biases in sex ratios, the capacity of natural enemies to shift or further skew operational sex ratios following sex allocation and parental care remains largely unstudied in natural populations. Male cocoons of the sawfly Neodiprion abietis (Hymenoptera: Diprionidae) are consistently smaller than those of females, with very little overlap, and thus, we were able to use cocoon size to sex cocoons. We studied three consecutive cohorts of N. abietis in six forest stands to detect cocoon volume‐associated biases in the attack of predators, pathogens, and parasitoids and examine how the combined effect of natural enemies shapes the realized operational sex ratio. Neodiprion abietis mortality during the cocoon stage was sex‐biased, being 1.6 times greater for males than females. Greater net mortality in males occurred because male‐biased mortality caused by a pteromalid parasitic wasp and a baculovirus was greater and more skewed than female‐biased mortality caused by ichneumonid parasitic wasps. Variation in the susceptibility of each sex to each family of parasitoids was associated with differences in size and life histories of male and female hosts. A simulation based on the data indicated that shifts in the nature of differential mortality have different effects on the sex ratio and fitness of survivors. Because previous work has indicated that reduced host plant foliage quality induces female‐biased mortality in this species, bottom‐up and top‐down factors acting on populations can affect operational sex ratios in similar or opposite ways. Shifts in ecological conditions therefore have the potential to alter progeny fitness and produce extreme sex ratio skews, even in the absence of unbalanced sex allocation. This would limit the capacity of females to anticipate the operational sex ratio and reliably predict the reproductive success of each gender at sex allocation.

Highlights

Sex ratio at maturity, hereafter referred to as operational sex ratio (OSR), influences competition for mates and reproductive output (Darwin, 1871), as well as sexual selection under some circumstances (Klug, Heuschele, Jennions, & Kokko, 2010)
It is assumed that sex-biased mortality may be induced in hymenopterans by pathogens, predators, and parasitoids, but evidence has come from either (1) laboratory experiments (Kapranas, Wajnberg, & Luck, 2009; Lin & Ives, 2003; Salt, 1935); (2) field studies in which sex biases cannot be unambiguously attributed to the action of natural enemies because host population sex ratio prior to their action was undetermined (Bird, 1961; Carne, 1969; Griffiths, 1959; Houseweart & Kulman, 1976); or (3) manipulated field studies using a single type of enemy (Holling, 1958; Yearian, Young, & Livingston, 1973), disregarding other enemies that may have negated or increased sex biases in natural conditions
We identified all adult parasitoids emerging in the laboratory from N. abietis cocoons by comparisons with voucher specimens from the Canadian National Collection (CNC), Ottawa

Summary

| INTRODUCTION

Hereafter referred to as operational sex ratio (OSR), influences competition for mates and reproductive output (Darwin, 1871), as well as sexual selection under some circumstances (Klug, Heuschele, Jennions, & Kokko, 2010). By contrast with the primary sex ratio, the ratio at fertilization that is under direct control of natural selection (see reviews in Charnov, 1982; Hardy, 2002; Wrensch & Ebbert, 1993), OSR and the proximate causes of OSR bias after parental investment ended (i.e., juvenile, sex-biased mortality) are poorly understood and have been the subject of few field studies. In ecological studies conducted with Neodiprion abietis (Harris) (Hymenoptera: Diprionidae) (Figure 1), a univoltine arrhenotokous sawfly with discrete generations (i.e., no parental care), OSRs ranged from 0.59 to 4.00 males per female (M:F) (Moreau, 2004) This wide range of OSRs could be attributed to unbalanced sex allocation, previous studies (Carroll, 1962; Moreau et al, 2003) have shown that cohorts collected from undefoliated host plants generally exhibited female-biased sex ratios when successfully reared (i.e., low mortality) in the absence of natural enemies, suggesting that male-biased sex ratios are probably due, at least in part, to female-biased mortality in juveniles.

| MATERIALS AND METHODS

Findings

| DISCUSSION