Females Manipulate Behavior of Caring Males Via Prenatal Maternal Effects
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Females manipulate behavior of caring males via prenatal maternal effects Matthieu Paqueta,1 and Per T. Smisetha aInstitute of Evolutionary Biology, School of Biological Sciences, The University of Edinburgh, Edinburgh EH9 3FL, United Kingdom Edited by Tom Tregenza, University of Exeter, Cornwall, Penryn, United Kingdom, and accepted by Editorial Board Member Douglas Futuyma May 11, 2017 (received for review December 1, 2016) In species with biparental care, there is sexual conflict as each (9–11), thereby providing a potential tool for manipulating the parent is under selection to minimize its personal effort by shifting behavior of caring males. For example, by producing smaller eggs, as much as possible of the workload over to the other parent. females could redirect the costs of parental care from the prenatal Most theoretical and empirical work on the resolution of this period, when they pay the full costs of egg production, toward the conflict has focused on strategies used by both parents, such as postnatal period, when the costs of rearing young are shared with negotiation. However, because females produce the eggs, this the male (9). Alternatively, females may deposit yolk androgens might afford females with an ability to manipulate male behavior that modulate offspring begging behavior in a way that alters the via maternal effects that alter offspring phenotypes. To test this male’s perception of offspring need, thereby increasing male hypothesis, we manipulated the prenatal conditions (i.e., presence contributions to care (9–11). Thus, if prenatal maternal effects or absence of the male), performed a cross-fostering experiment, influence the resolution of sexual conflict over care, this would and monitored the subsequent effects of prenatal conditions on introduce an asymmetry of power between the two sexes, with the Nicro- offspring and parental performance in the burying beetle female gaining the upper hand. phorus vespilloides . We found that offspring were smaller at At present, we lack conclusive evidence as to whether females hatching when females laid eggs in presence of a male, suggesting can use prenatal maternal effects to manipulate the behavior of that females invest less in eggs when expecting male assistance. caring males (12–16). A main reason for this is that it is difficult Furthermore, broods laid in the presence of a male gained more to demonstrate female manipulation, owing to several chal- weight during parental care, and they did so at the expense of lenges. First, females could manipulate males via several mech- male weight gain. Contrary to our expectations, males cared less anisms, including yolk androgens, other egg components, egg for broods laid in the presence of a male. Our results provide size, and egg coloration (4), and thus existing experimental de- experimental evidence that females can alter male behavior dur- ing breeding by adjusting maternal effects according to prenatal signs that focus on specific mechanisms risk targeting the wrong conditions. However, rather than increasing the male’s parental mechanism. Second, to demonstrate that prenatal maternal ef- effort, females appeared to suppress the male’s food consump- fects alter male behavior, it is essential to separate the effects of tion, thereby leaving more food for their brood. prenatal conditions from those of postnatal conditions. Third, there may be a limited time window for maternal manipulation, food consumption | manipulation | maternal effects | parental care | because maternal effects on offspring behavior often wane as – sexual conflict offspring develop (17 19). Fourth, in addition to sexual conflict over parental care, there may be sexual conflict over food con- n species where parents cooperate to care for their joint off- sumption from shared resources (20, 21). Finally, to demonstrate Ispring (as long as there is scope for divorce and/or remating following the partner’s death), there will be sexual conflict over Significance parental care, with each parent being under selection to mini- mize its own effort and shift as much as possible of the workload In biparental species, sexual conflict arises as each parent at- to its partner (1). Previous empirical and theoretical work has tempts to minimize its personal effort. Most work has focused focused mainly on three behavioral mechanisms that may me- on how this conflict is resolved through symmetrical decisions diate the resolution of this conflict (1, 2). First, incomplete between parents. We investigated whether females can influ- compensation, or negotiation, occurs when each parent increases ence male decisions by altering the offspring’s phenotype via its level of care in response to a reduction in its partner’s con- the eggs. We manipulated the prenatal presence of the male, tribution, but such that it does not fully correspond to its part- performed a cross-fostering experiment, and monitored the ner’s reduction (3). Second, matching occurs when each parent subsequent effects on offspring and parent performance. Off- adjusts its level of care to its partner’s contribution by matching spring laid in presence of a male were smaller at hatching. In any increase or reduction in its partner’s contribution in the same addition, males lost more weight when with larvae laid in direction as its partner (4). Third, sealed bid models assume that presence of a male. Our results show that females can manip- each parent makes an initial fixed decision about how much care ulate male behavior, suggesting that prenatal maternal effects to provide irrespective of its partner’s decision (5). There is some can play an important role in the resolution of sexual conflict support for all three mechanisms from experimental studies on between parents. birds and other taxa (6–8); however, a meta-analysis of mate Author contributions: M.P. and P.T.S. designed research; M.P. performed research; M.P. removal and handicapping experiments on birds found the analyzed data; and M.P. and P.T.S. wrote the paper. greatest overall support for negotiation (2). The authors declare no conflict of interest. Our current understanding of the resolution of sexual conflict This article is a PNAS Direct Submission. T.T. is a guest editor invited by the Editorial suggest that males and females use the same behavioral strategies Board. for resolving conflict (e.g., negotiation) (9). However, given that Data deposition: The results from this paper are available through Dryad (doi:10.5061/ females produce the eggs, they might use their control over egg dryad.8424c). production as a mechanism for biasing conflict resolution in their 1To whom correspondence should be addressed. Email: [email protected]. favor. In many species, females deposit hormones and/or nutrients This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. into the eggs that alter the offspring’s behavior or development 1073/pnas.1619759114/-/DCSupplemental. 6800–6805 | PNAS | June 27, 2017 | vol. 114 | no. 26 www.pnas.org/cgi/doi/10.1073/pnas.1619759114 Downloaded by guest on September 30, 2021 female manipulation, it is crucial to document fitness benefits to females and/or offspring and fitness costs to males (4). Here we report an experiment on the burying beetle Nicro- phorus vespilloides, an insect exhibiting facultative biparental care (22). This species is ideal for studying female manipulation of male behavior because it allows us to address all five chal- lenges listed above. First, we used a new experimental approach in which we targeted prenatal environmental conditions expec- ted to influence female decisions on maternal effects and then monitored downstream consequences for offspring size at hatch- ing, male and female care, and male, female, and offspring fitness (9). Here we targeted a prenatal environmental condition that is essential for female manipulation of males: the presence or ab- sence of the male during egg laying. Second, we conducted a cross-fostering experiment to separate prenatal and postnatal effects by giving each pair of beetles an experimental brood of newly hatched larvae derived from one of our two treatment groups. In one treatment, larvae derived from eggs laid when the male was present during egg laying, whereas in the other treat- ment, larvae derived from eggs laid when the male was absent during egg laying. Third, we recorded parental behaviors over 3 consecutive days, covering the full duration of parental care from hatching until nutritional independence (23). Fourth, we investigated sexual conflict over both parental care and food consumption from a resource shared by both parents and their Fig. 1. Maternal effect of the presence of the male before hatching on offspring (i.e., a small vertebrate carcass). To this end, we brood weight at hatching. Raw data and associated mean ± SE values are recorded the body mass of males and females before and after shown for brood weight of larvae laid in absence of a male (black open breeding. Finally, we monitored subsequent effects on post- circles; n = 30) and brood weight of larvae laid in presence of a male (red breeding survival of males and females as well as offspring filled circles; n = 31). (Inset) Predicted mean ± SE values from the final model. growth and survival across different life stages. Each experimental brood comprised 20 larvae mixed from different donor pairs of the same prehatching treatment that were not the larvae’s foster Results parents. We weighed the 20 larvae together before placing them on the We found evidence for a prenatal maternal effect on offspring carcass as a measure of prenatal maternal investment. size at hatching owing to the presence or absence of the male during laying. Females that laid eggs in the presence of a male caring males by suppressing male food consumption from the partner produced larvae that were 3.4% lighter at hatching shared resource. compared with larvae from females who laid eggs in the absence We found no evidence that maternal effects influenced the of a male (estimated mean ± SE, 1.85 ± 0.826 mg; F = 5.02; 1,59 behavior of caring females.