Polyandrous Bee Provides Extended Offspring Care Biparentally As an Alternative to Monandry Based Eusociality
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Polyandrous bee provides extended offspring care biparentally as an alternative to monandry based eusociality Michael Mikáta,1, Lukáš Janošíkb, Katerina Cerná a, Eva Matouškováa,Jirí Hadravaa,c, Vít Bureša, and Jakub Strakaa aDepartment of Zoology, Faculty of Science, Charles University, CZ-12844 Prague, Czech Republic; bDepartment of Botany, Faculty of Science, Charles University, CZ-12801 Prague, Czech Republic; and cInstitute of Entomology, Biological Centre, Czech Academy of Science, CZ-370 05 Ceské Budejovice, Czech Republic Edited by Raghavendra Gadagkar, Indian Institute of Science, Bangalore, India, and approved February 12, 2019 (received for review June 12, 2018) Parental care behavior evolves to increase the survival of off- Monopolization of multiple females is usually the most beneficial spring. When offspring care becomes complicated for ecological strategy for males; however, when this is not possible, it is best for reasons, cooperation of multiple individuals can be beneficial. males to monopolize at least one female (15). This situation There are two types of cooperative care: biparental care and typically occurs in species with low population density (as indi- worker (helper)-based care (e.g., eusociality). Although biparental viduals rarely meet) (19) or with male-biased sex ratios (as most of care is common in several groups of vertebrates, it is generally rare the females are occupied by other males) (20). Mate guarding of a in arthropods. Conversely, eusociality is widespread in insects, single female leads to social monogamy. Social monogamy is an especially the aculeate Hymenoptera. Here, we present a case of association between a single male and a single female, which can biparental care in bees, in Ceratina nigrolabiata (Apidae, Xyloco- last for the whole reproductive life or only temporarily (21). Male pinae). Similar to eusocial behavior, biparental care leads to participation in offspring care can be a byproduct of mate guarding greater brood protection in this species. Male guarding increases (19, 22). In this situation, no tradeoff between care and mating provisioning of nests because females are liberated from the trade- opportunities occurs. In the case of social monogamy, investment into parental care is beneficial for the male because he is less likely off between provisioning and nest protection. The main benefit of EVOLUTION parental care for males should be increased paternity. Interestingly to gain from interactions with other females (15). It is important to though, we found that paternity of offspring by guard males is remember that social monogamy does not necessarily mean ge- extraordinarily low (10% of offspring). Generally, we found that netic monogamy: extrapair copulation is not uncommon (21, 23). Here, we describe biparental care in the solitary apid bee, nests were not guarded by the same male for the whole provision- Ceratina nigrolabiata, which represents a case of biparental care ing season, meaning that males arrive to nests as stepfathers. How- in bees. Bees and most other aculeate Hymenoptera have spe- ever, we show that long-term guarding performed by a single male cific natural history traits that can strongly modulate the evolu- does increase paternity. We suggest that the multiple-mating strat- tion of parental care, including (i) nest-making behavior; (ii) egy of these bees increased the amount of time for interactions haplodiploid sex determination, in which males only genetically between the sexes, and this longer period of potential interaction participate in female offspring; and (iii) a spermatheca, which supported the origin of biparental care. Eusociality based on mon- allows the female to store sperm for months or even years (24). andry was thought to be the main type of extended brood pro- Parallel evolution of biparental care in C. nigrolabiata and Try- tection in bees. We show that biparental care based on polyandry poxylon crabronid wasps is likely, as Trypoxylon and Ceratina provides an interesting evolutionary alternative. Significance biparental care | social behavior | paternity | mating frequency | bees Biparental care is a rare strategy of offspring protection in in- n biparental care, females and males cooperate in the care of sects. We discovered a case of biparental care in bees, in Ioffspring (1, 2). Several aspects of offspring care can influence Ceratina nigrolabiata. Benefits of biparental care were identi- the evolution of biparental care: the synergistic effect of male fied for both males and females; yet, we found that an ex- and female care (3), the inability of one parent to care for off- traordinarily high proportion of offspring were unrelated to spring effectively (4), or care that has similar costs and benefits guard males. This is because females of C. nigrolabiata are for both sexes (5, 6). Biparental care is relatively common among polyandrous and store sperm. Therefore, the most important vertebrates: it is the dominant type in birds (1) and frequently benefit for males is increased mating opportunities. We sug- occurs in mammal, amphibian, and fish lineages (7). Conversely, gest that female polyandry and prolonged female receptivity biparental care is very rare among arthropods, with only a few supported the origin and/or maintenance of biparental care known examples, including cockroaches from the genus Crypto- concomitant with extended male lifespan. Biparental care is an cercus, as well as burying, passalid, and bark beetles (2, 4, 8). Bi- alternative method of brood protection to eusociality, which parental care has also been documented in crabronid wasps of the provides similar benefits but arises under different female genus Trypoxylon (subgenus Trypargillum) belonging to the aculeate mating conditions. Hymenoptera (9, 10). Generally, in this group of insects, females perform nest provisioning, while males perform nest guarding and Author contributions: M.M., K.C., and J.S. designed research; M.M., L.J., K.C., E.M., V.B., help with nest construction (10, 11). Among the aculeate Hyme- and J.S. performed research; M.M. and J.H. analyzed data; and M.M., J.H., and J.S. wrote noptera, male participation in offspring care is rare (2, 12). On the the paper. other hand, the occurrence of extensive female care is common, The authors declare no conflict of interest. and there have been several origins of eusociality (12–14). This article is a PNAS Direct Submission. Male and female mating strategies are strongly related to the Published under the PNAS license. type of parental care (15, 16). Males, in contrast to females, 1To whom correspondence should be addressed. Email: [email protected]. usually benefit more from an increased number of copulation This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. events than from substantial investment in offspring care (17, 18). 1073/pnas.1810092116/-/DCSupplemental. Male behavior can be further influenced by female availability. www.pnas.org/cgi/doi/10.1073/pnas.1810092116 PNAS Latest Articles | 1of6 Downloaded by guest on September 24, 2021 share natural history traits typical of nest-making aculeate Hy- Experimental Removal of Males from Their Nests. When a C. menoptera (9–11). As biparental care should increase the fitness nigrolabiata male was removed from a nest, he was replaced by an- of both sexes (2, 6), we tested the benefits of this strategy for other male within the first day postremoval in 61% of cases (47 out of males and females separately. We identified the maternity and 77 nests; SI Appendix,TableS2). By the fourth day after removal, the paternity of brood individuals using microsatellites, and we proportion of nests with a guard male did not significantly differ compared the mating frequency of C. nigrolabiata with that of between manipulated and control nests (Fisher’sexacttest,P = 0.153; solitary and facultatively eusocial bee species in which single n = 76; SI Appendix,TableS2). Removal of the male was not asso- mating is known (14, 25–27). Importantly, the presence of soli- ciated with the presence of brood cell damage (Fisher’s exact test, P = tary, biparental, and eusocial nesting within the same bee genus 0.694; n = 162); however, it did result in decreased nesting pro- allows for comparisons of the existing cooperative strategies. ductivity in nests where the couple was successfully reestablished, as measured by the number of eggs (Fig. 2D; GLM Poisson, df = Results 1, deviance = 5.09, P = 0.024, n = 73) and the number of offspring – – (at or before the third larval stage; Fig. 2E; GLM Poisson, df = 1, Presence of a Male Female Pair in Active Brood Nests. Amale = = = female pair was found in 88% of the active brood nests of C. deviance 5.59, P 0.015, n 73). Interestingly, male removal nigrolabiata (404 out of 460; SI Appendix, Table S1). In 1% of the had a significant influence on female behavior. Females in male- active brood nests (5 out of 460; SI Appendix, Table S1), one removed nests performed fewer foraging trips [in 1.5 h of obser- female and multiple males were present. In the remaining nests, vation time post-male removal; Fig. 3A; paired Wilcoxon test, V (test criterium of Wilcoxon paired test) = 221, P = 0.002; n = 24], there were only adults of a single sex (only a male in 5%: 26 out and they spent less time outside their nests (Fig. 3B and Table 1; of 404 nests; only a female in 4%: 18 out of 404 nests; SI Ap- paired Wilcoxon test, V = 264, P < 0.001; n = 24). pendix, Table S1) or no adults at all (2%: 8 out of 404 nests; SI Appendix, Table S1). We did not observe any nest with more than Experimental Removal of Females from Their Nests. Removal of C. one adult female. nigrolabiata females had a significant effect on the departure of guard There was a pronounced division of labor between males males (Fisher’s exact test, P < 0.001; n = 94).