• This record comes from PubMed

Polyandrous bee provides extended offspring care biparentally as an alternative to monandry based eusociality

. 2019 Mar 26 ; 116 (13) : 6238-6243. [epub] 20190311

Language English Country United States Media print-electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Parental care behavior evolves to increase the survival of offspring. When offspring care becomes complicated for ecological reasons, cooperation of multiple individuals can be beneficial. There are two types of cooperative care: biparental care and worker (helper)-based care (e.g., eusociality). Although biparental care is common in several groups of vertebrates, it is generally rare in arthropods. Conversely, eusociality is widespread in insects, especially the aculeate Hymenoptera. Here, we present a case of biparental care in bees, in Ceratina nigrolabiata (Apidae, Xylocopinae). Similar to eusocial behavior, biparental care leads to greater brood protection in this species. Male guarding increases provisioning of nests because females are liberated from the tradeoff between provisioning and nest protection. The main benefit of parental care for males should be increased paternity. Interestingly though, we found that paternity of offspring by guard males is extraordinarily low (10% of offspring). Generally, we found that nests were not guarded by the same male for the whole provisioning season, meaning that males arrive to nests as stepfathers. However, we show that long-term guarding performed by a single male does increase paternity. We suggest that the multiple-mating strategy of these bees increased the amount of time for interactions between the sexes, and this longer period of potential interaction supported the origin of biparental care. Eusociality based on monandry was thought to be the main type of extended brood protection in bees. We show that biparental care based on polyandry provides an interesting evolutionary alternative.

Comment In

PubMed

Comment In

PubMed

See more in PubMed

Cockburn A. Prevalence of different modes of parental care in birds. Proc Biol Sci. 2006;273:1375–1383. PubMed PMC

Suzuki S. Biparental care in insects: Paternal care, life history, and the function of the nest. J Insect Sci. 2013;13:131. PubMed PMC

Fromhage L, Jennions MD. Coevolution of parental investment and sexually selected traits drives sex-role divergence. Nat Commun. 2016;7:12517. PubMed PMC

Tallamy DW, Wood TK. Convergence patterns in subsocial insects. Annu Rev Entomol. 1986;31:369–390.

McNamara JM, Wolf M. Sexual conflict over parental care promotes the evolution of sex differences in care and the ability to care. Proc Biol Sci. 2015;282:20142752. PubMed PMC

Westneat DF, Craig Sargent R. Sex and parenting: The effects of sexual conflict and parentage on parental strategies. Trends Ecol Evol. 1996;11:87–91. PubMed

Reynolds JD, Goodwin NB, Freckleton RP. Evolutionary transitions in parental care and live bearing in vertebrates. Philos Trans R Soc Lond B Biol Sci. 2002;357:269–281. PubMed PMC

Gilbert JDJ, Manica A. The evolution of parental care in insects: A test of current hypotheses. Evolution. 2015;69:1255–1270. PubMed PMC

Bergamaschi ACB, Almeida JDC, Campos LADO, Del Lama MA. Sociogenetic structure in nests of the mud dauber wasp Trypoxylon (Trypargilum) albitarse (Hymenoptera: Crabronidae) Eur J Entomol. 2015;112:722–727.

Brockmann HJ, Grafen A. Mate conflict and male behaviour in a solitary wasp, Trypoxylon (Trypargilum) politum (Hymenoptera: Sphecidae) Anim Behav. 1989;37:232–255.

Brockmann HJ. Male behavior, courtship and nesting in Trypoxylon (Trypargilum) monteverdeae (Hymenoptera: Sphecidae) J Kans Entomol Soc. 1992;65:66–84.

Korb J, Heinze J. Major hurdles for the evolution of sociality. Annu Rev Entomol. 2016;61:297–316. PubMed

Wilson EO. The Insect Societies. Belknap Press of Harvard Univ Press; Cambridge, MA: 1971. pp. 75–102.

Hughes WO, Oldroyd BP, Beekman M, Ratnieks FL. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science. 2008;320:1213–1216. PubMed

Emlen ST, Oring LW. Ecology, sexual selection, and the evolution of mating systems. Science. 1977;197:215–223. PubMed

Liker A, Freckleton RP, Remeš V, Székely T. Sex differences in parental care: Gametic investment, sexual selection, and social environment. Evolution. 2015;69:2862–2875. PubMed

Queller DC. Why do females care more than males? Proc R Soc Lond B Biol Sci. 1997;264:1555–1557.

Royle NJ. Parental care: When the sex has to stop. Curr Biol. 2016;26:R478–R480. PubMed

Lukas D, Clutton-Brock TH. The evolution of social monogamy in mammals. Science. 2013;341:526–530. PubMed

Harts AM, Kokko H. Understanding promiscuity: When is seeking additional mates better than guarding an already found one? Evolution. 2013;67:2838–2848. PubMed

Cohas A, Allainé D. Social structure influences extra-pair paternity in socially monogamous mammals. Biol Lett. 2009;5:313–316. PubMed PMC

Van Rhijn JG. Mate guarding as a key factor in the evolution of parental care in birds. Anim Behav. 1991;41:963–970.

Petrie M, Kempenaers B. Extra-pair paternity in birds: Explaining variation between species and populations. Trends Ecol Evol. 1998;13:52–58. PubMed

Michener CD. The Bees of the World. 2nd Ed. Johns Hopkins Univ Press; Baltimore: 2007. pp. 6–11.

Paxton RJ. Male mating behaviour and mating systems of bees: An overview. Apidologie. 2005;36:145–156.

Alcock J. Sexual selection and the mating behavior of solitary bees. In: Brockmann HJ, Naguib TJRM, Mitani JC, Simmons LW, Barrett L, editors. Advances in the Study of Behavior. Academic; 2013. pp. 1–48.

Shell WA, Rehan SM. The price of insurance: Costs and benefits of worker production in a facultatively social bee. Behav Ecol. 2017;29:204–211.

Mikát M, Černá K, Straka J. Major benefits of guarding behavior in subsocial bees: Implications for social evolution. Ecol Evol. 2016;6:6784–6797. PubMed PMC

Coville RE, Griswold C, Coville PL. Observations on the nesting biology and behavior of Trypoxylon (Trypargilum) vagulum (Hymenoptera: Sphecidae) in Costa Rica. Pan-Pac Entomol. 2000;76:28–48.

Gerling D, Hurd PD, Hefetz A. Comparative Behavioral Biology of Two Middle East Species of Carpenter Bees (Xylocopa Latreille)(Hymenoptera: Apoidea) Smithsonian Institution Scholarly Press; Washington, DC: 1983. pp. 1–33.

Rehan SM, Richards MH, Adams M, Schwarz MP. The costs and benefits of sociality in a facultatively social bee. Anim Behav. 2014;97:77–85.

Stark RE. Cooperative nesting in the multivoltine large carpenter bee Xylocopa sulcatipes Maa (Apoidea: Anthophoridae): Do helpers gain or lose to solitary females? Ethology. 1992;91:301–310.

Clouse R. Some effects of group size on the output of beginning nests of Mischocyttarus mexicanus (Hymenoptera: Vespidae) Fla Entomol. 2001;84:418.

Richards MH, Packer L. Demography and relatedness in multiple-foundress nests of the social sweat bee, Halictus ligatus. Insectes Soc. 1998;45:97–109.

Andersson M. The evolution of eusociality. Annu Rev Ecol Syst. 1984;15:165–189.

Hogendoorn K, Velthuis HHW. The role of young guards in Xylocopa pubescens. Insectes Soc. 1995;42:427–448.

Mikát M, Franchino C, Rehan SM. Sociodemographic variation in foraging behavior and the adaptive significance of worker production in the facultatively social small carpenter bee, Ceratina calcarata. Behav Ecol Sociobiol. 2017;71:135.

Barber CA, Robertson RJ, Boag PT. The high frequency of extra-pair paternity in tree swallows is not an artifact of nestboxes. Behav Ecol Sociobiol. 1996;38:425–430.

Mulder RA, Dunn PO, Cockburn A, Lazenby-Cohen KA, Howell MJ. Helpers liberate female fairy-wrens from constraints on extra-pair mate choice. Proc R Soc Lond B Biol Sci. 1994;255:223–229.

Kokko H, Jennions MD. Parental investment, sexual selection and sex ratios. J Evol Biol. 2008;21:919–948. PubMed

Stubblefield JW, Seger J. The Differences Between the Sexes. Cambridge Univ Press; Cambridge, UK: 1994. Sexual Dimorphism in the Hymenoptera; pp. 71–103.

Rehan SM, Richards MH. Nesting biology and subsociality in Ceratina calcarata (Hymenoptera: Apidae) Can Entomol. 2010;142:65–74.

Gotthard K, Nylin S, Wiklund C. Mating opportunity and the evolution of sex-specific mortality rates in a butterfly. Oecologia. 2000;122:36–43. PubMed

Heinze J. The male has done his work - the male may go. Curr Opin Insect Sci. 2016;16:22–27. PubMed

Rehan SM, Leys R, Schwarz MP. A mid-cretaceous origin of sociality in xylocopine bees with only two origins of true worker castes indicates severe barriers to eusociality. PLoS One. 2012;7:e34690. PubMed PMC

Kalinowski ST, Taper ML, Marshall TC. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol. 2007;16:1099–1106. PubMed

Jones OR, Wang J. COLONY: A program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour. 2010;10:551–555. PubMed

R. Core Developmental Team 2016. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna), Version 3.2.5.

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...