Skip to main content
SpringerLink
Log in

Sex-biased parental care and sexual size dimorphism in a provisioning arthropod

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

The diverse selection pressures driving the evolution of sexual size dimorphism (SSD) have long been debated. Whilst the balance between fecundity selection and sexual selection has received much attention, explanations based on sex-specific ecology have proven harder to test. In ectotherms, females are typically larger than males, and this is frequently thought to be because size constrains female fecundity more than it constrains male mating success. However, SSD could additionally reflect maternal care strategies. Under this hypothesis, females are relatively larger where reproduction requires greater maximum maternal effort—for example where mothers transport heavy provisions to the nests. To test this hypothesis, we focussed on digger wasps (Hymenoptera: Ammophilini), a relatively homogeneous group in which only females provision offspring. In some species, a single large prey item, up to ten times the mother’s weight, must be carried to each burrow on foot; other species provide many small prey, each flown individually to the nest. We found more pronounced female-biased SSD in species where females carry single, heavy prey. More generally, SSD was negatively correlated with the numbers of prey provided per offspring. Females provisioning multiple small items had longer wings and thoraxes, probably because smaller prey are carried in flight. Despite much theorising, few empirical studies have tested how sex-biased parental care can affect SSD. Our study reveals that such costs can be associated with the evolution of dimorphism, and this should be investigated in other clades where parental care costs differ between sexes and species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Baerends GP (1941) Fortpflanzungsverhalten und orientierung der grabwespe Ammophila campestris Jur. Tijdschr Entomol 84:68–275

    Google Scholar 

  • Berry JF, Shine R (1980) Sexual size dimorphism and sexual selection in turtles (order Testudines). Oecologia 44:185–191

    Article  Google Scholar 

  • Blanckenhorn WU (2005) Behavioral causes and consequences of sexual size dimorphism. Ethology 111:977–1016

    Article  Google Scholar 

  • Blanckenhorn WU, Dixon AFG, Fairbairn DJ, Foellmer MW, Gibert P, van der Linde K, Meier R, Nylin S, Pitnick S, Schoff C, Signorelli M, Teder T, Wiklund C (2007) Proximate causes of Rensch’s rule: does sexual size dimorphism in arthropods result from sex differences in development time? Am Nat 169:245–257

    Article  PubMed  Google Scholar 

  • Blösch M (2000) Die Grabwespen Deutschlands. Goecke & Evers, Keltern

    Google Scholar 

  • Bohart RM, Menke AS (1976) Sphecid wasps of the world: a generic revision. Univ California Press, Berkeley

    Google Scholar 

  • Chippendale AK, Gibson JR, Rice WR (2001) Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc Natl Acad Sci U S A 98(4):1671–1675

    Article  Google Scholar 

  • Choe JC, Crespi BJ (eds) (1997) The evolution of social behaviour in insects and arachnids. Cambridge University Press, Cambridge

    Google Scholar 

  • Clutton-Brock TH, Harvey PH, Rudder B (1977) Sexual size dimorphism, socionomic sex ratio and body weight in primates. Nature 269:797–800

    Article  CAS  PubMed  Google Scholar 

  • Coelho JR (1997) Sexual size dimorphism and flight behavior in cicada killers (Sphecius speciosus). Oikos 79:371–375

    Article  Google Scholar 

  • Costa JC (2006) The other insect societies. Belknap/Harvard, Cambridge

    Google Scholar 

  • Cox RM (2006) A test of the reproductive cost hypothesis for sexual size dimorphism in Yarrow’s spiny lizard Sceloporus jarrovii. J Anim Ecol 75(6):1361–1369

    Article  CAS  PubMed  Google Scholar 

  • De Groot W (1974) Een in kevergaten nestelende Ammophila, A. clypeata (Hym., Sphecidae). Entomol Ber 34:24–28

    Google Scholar 

  • del Castillo RC, Fairbairn DJ (2012) Macroevolutionary patterns of bumblebee body size: detecting the interplay between natural and sexual selection. Ecol Evol 2(1):46–57

    Article  PubMed Central  PubMed  Google Scholar 

  • Dollfuss H (2015) Revision of the wasp genus Ammophila KIRBY 1798 (Hymenoptera: Apoidea: Sphecidae) of the Sub-Saharan region of Africa. Linzer Biol Beiträge 47:307–412

    Google Scholar 

  • Edwards PB, Aschenborn HH (1989) Maternal care of a single offspring in the dung beetle Kheper nigroaeneus: the consequences of extreme parental investment. J Nat Hist 23(1):17–27

    Article  Google Scholar 

  • Evans HE (1959) Observations on the nesting behavior of digger wasps of the genus Ammophila. Am Midl Nat 62:449–473

    Article  Google Scholar 

  • Evans HE (1965) Simultaneous care of more than one nest by Ammophila azteca Cameron (Hymenoptera: Sphecidae). Psyche 72:8–23

    Article  Google Scholar 

  • Evans HE (1969) Phoretic copulation in the Hymenoptera. Entomol News 80:113–124

    Google Scholar 

  • Fairbairn DJ (1997) Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annu Rev Ecol Syst 28:659–687

    Article  Google Scholar 

  • Fairbairn DJ, Preziozi RF (1994) Sexual selection and the evolution of allometry for sexual size dimorphism in the water strider, Aquarius remigis. Am Nat 144:101–118

    Article  Google Scholar 

  • Fairbairn DJ, Blanckenhorn WU, Szekely T (2007) Sex, size and gender roles: evolutionary studies of sexual size dimorphism. Oxford University Press, New York

    Book  Google Scholar 

  • Favila ME (1993) Some ecological factors affecting the life-style of Canthon cyanellus cyanellus (Coleoptera Scarabaeidae): an experimental approach. Ethol Ecol Evol 5(3):319–328

    Article  Google Scholar 

  • Field J (1989) Intraspecific parasitism and nesting success in the solitary wasp Ammophila sabulosa. Behaviour 110:23–45

    Article  Google Scholar 

  • Field J (1992a) Patterns of nest provisioning and parental investment in the solitary digger wasp Ammophila sabulosa. Ecol Entomol 17:43–51

    Article  Google Scholar 

  • Field J (1992b) Prey utilization by the solitary digger wasp Ammophila sabulosa (Linnaeus) (Hymenoptera: Sphecidae). Entomol Gazette 43:131–138

    Google Scholar 

  • Field J (1993) Nesting biology of the solitary digger wasp Podalonia affinis (K.) (Hymenoptera: Sphecidae). Entomologist 112:17–24

    Google Scholar 

  • Field J, Turner E, Fayle T, Foster WA (2007) Costs of egg-laying and offspring provisioning: multifaceted parental investment in a digger wasp. Proc R Soc Lond B 274:445–451. doi:10.1098/Rspb.2006.3745

    Article  Google Scholar 

  • Field J, Ohl M, Kennedy M (2011) A molecular phylogeny for digger wasps in the tribe Ammophilini (Hymenoptera, Apoidea, Sphecidae. Syst Entomol 36:732–740. doi:10.1111/J.1365-3113.2011.00591.X

    Article  Google Scholar 

  • Gaimari SD, Martins RP (1996) Nesting behavior and nest distributions of Ammophila gracilis Lepeletier (Hymenoptera: Sphecidae) in Brazil. J Hymenopt Res 5:240–248

    Google Scholar 

  • Gilbert JJ (1983) Sexual dimorphism in zooplankton (Copepoda, Cladocera, and Rotifera). Annu Rev Ecol Syst 14:1–33

    Article  Google Scholar 

  • Gilbert JDJ (2011) Insect dry weight: shortcut to a difficult quantity using museum specimens. Fla Entomol 94(4):964–970

    Article  Google Scholar 

  • Gilbert JDJ, Manica A (2015) The evolution of parental care in insects: a test of current hypotheses. Evolution 69(5):1255–1270

    Article  PubMed Central  PubMed  Google Scholar 

  • Goubault M, Scott D, Hardy IC (2007) The importance of offspring value: maternal defence in parasitoid contests. Anim Behav 74(3):437–446

    Article  Google Scholar 

  • Halffter G (1997) Subsocial behavior in Scarabaeinae beetles. In: Choe J, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge

    Google Scholar 

  • Han X, Fu J (2013) Does life history shape sexual size dimorphism in anurans? A comparative analysis. BMC Evol Biol 13(1):27

    Article  PubMed Central  PubMed  Google Scholar 

  • Head G (1995) Selection on fecundity and variation in the degree of sexual size dimorphism among spider species (class Araneae). Evolution 49:776–781

    Article  Google Scholar 

  • Hedrick AV, Temeles EJ (1989) The evolution of sexual dimorphism in animals: hypotheses and tests. Trends Ecol Evol 4(5):136–138

    Article  CAS  PubMed  Google Scholar 

  • Herrel A, Spithoven L, Van Damme R, De Vree F (1999) Sexual dimorphism of head size in Gallotia galloti: testing the niche divergence hypothesis by functional analyses. Funct Ecol 13(3):289–297

    Article  Google Scholar 

  • Hicks CH (1934) Biological notes on Sphex wrightii (Cresson). Psyche 41:150–157

    Article  Google Scholar 

  • Hinton HE (1981) Biology of insect eggs, vol 1. Pergamon, Oxford

    Google Scholar 

  • Hunt J, Simmons LW, Kotiaho JS (2002) A cost of maternal care in the dung beetle Onthophagus taurus? J Evol Biol 15(1):57–64

    Article  Google Scholar 

  • Hurlbutt B (1987) Sexual size dimorphism in parasitoid wasps. Biol J Linn Soc 30:63–89

    Article  Google Scholar 

  • Iglesias MS, Crespo FA, Valverde ADC (2012) Is parental care behavior in Belostoma species an evolutionary cause for their common sexual size dimorphism pattern? Entomol Sci 15(2):155–161

    Article  Google Scholar 

  • Kazenas VL (1971) The biology of the fossorial wasp Ammophila (Eremochares) dives Brullé (Hymenoptera, Sphecidae). Entomol Rev 49:172–180

    Google Scholar 

  • Krüger O (2005) The evolution of reversed sexual size dimorphism in hawks, falcons and owls: a comparative study. Evol Ecol 19(5):467–486

    Article  Google Scholar 

  • Kurczewski FE, Spofford MG (1998) Alternative nesting strategies in Ammophila urnaria (Hymenoptera: Sphecidae). J Nat Hist 32:99–106

    Article  Google Scholar 

  • Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34(2):292–305

    Article  Google Scholar 

  • Lighton JR, Weier JA, Feener DH Jr (1993) The energetics of locomotion and load carriage in the desert harvester ant Pogonomyrmex rugosus. J Exp Biol 181:49–61

    Google Scholar 

  • Lindenfors P, Tullberg BS, Biuw M (2002) Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds. Behav Ecol Sociobiol 52:188–193

    Article  Google Scholar 

  • Lomholdt O (1984) The Sphecidae (Hymenoptera) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica vol 4, 2nd edn. Scandinavian Science Press, Denmark

    Google Scholar 

  • Marden JH (1987) Maximum lift production during takeoff in flying animals. J Exp Biol 130:235–258

    Google Scholar 

  • Monteith GB, Storey RI (1981) The biology of Cephalodesmius, a genus of dung beetles which synthesizes “dung” from plant material (Coleoptera: Scarabaeidae: Scarabaeinae). Mem Qld Mus 20(2):253–277

    Google Scholar 

  • Myers P (1978) Sexual dimorphism in size of vespertilionid bats. Am Nat 112(986):701–711

    Article  Google Scholar 

  • Nylin S, Wedell N (1994) Sexual size dimorphism and comparative methods. In: Eggleton P, Vane-Wright RI (eds) Phylogenetics and ecology. Academic, London

    Google Scholar 

  • O’Neill KM (1985) Egg size, prey size and sexual size dimorphism in digger wasps (Hymenoptera: Sphecidae). Can J Zool 63:2187–2193

    Article  Google Scholar 

  • O’Neill KM (2001) Solitary wasps. Cornell University Press, Ithaca

    Google Scholar 

  • O’Brien MF, O’Brien AM (1988) Biology of Ammophila evansi and A. mediata in Northern Michigan (Hymenoptera: Sphecidae). Pan-Pac Entomol 64:73–79

    Google Scholar 

  • Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2012) Caper: comparative analyses of phylogenetics and evolution in R. R package version 0.5. url: http://CRAN.R-project.org/package=caper

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Parker FD, Tepedino VJ, Vincent DL (1980) Observations on the provisioning behavior of Ammophila aberti Haldeman (Hymenoptera: Sphecidae. Psyche 87:249–258

    Article  Google Scholar 

  • Pavey CR (2008) Evolution of prey holding behaviour and large male body size in Ninox owls (Strigidae). Biol J Linn Soc 95(2):284–292

    Article  Google Scholar 

  • Petersson E (1995) Male load-lifting capacity and mating success in the swarming caddis fly Athripsodes cinereus. Physiol Entomol 20:66–70

    Article  Google Scholar 

  • Powell JA (1964) Additions to the knowledge of the nesting behavior of North American Ammophila (Hymenoptera: Sphecidae). J Kansas Entomol Soc 37:240–258

    Google Scholar 

  • Preziosi RF, Fairbairn DJ (2000) Lifetime selection on adult body size and components of body size in a waterstrider: opposing selection and maintenance of sexual size dimorphism. Evolution 54(2):558–566

    Article  CAS  PubMed  Google Scholar 

  • Ralls K (1976) Mammals in which females are larger than males. Q Rev Biol 51:245–276

    Article  CAS  PubMed  Google Scholar 

  • Ranta E, Laurila A, Elmberg J (1994) Reinventing the wheel—analysis of sexual dimorphism in body size. Oikos 70:313–321

    Article  Google Scholar 

  • Reimchen TE, Nosil P (2004) Variable predation regimes predict the evolution of sexual dimorphism in a population of threespine stickleback. Evolution 58(6):1274–1281

    Article  CAS  PubMed  Google Scholar 

  • Rosenheim JA (1987) Nesting-behavior and bionomics of a solitary ground-nesting wasp, Ammophila dysmica (Hymenoptera, Sphecidae)—influence of parasite pressure. Ann Entomol Soc Am 80:739–749

    Article  Google Scholar 

  • Rosenheim JA (1989) Behaviorally mediated spatial and temporal refuges from a cleptoparasite, Argochrysis armilla (Hymenoptera, Chrysididae), attacking a ground-nesting wasp, Ammophila dysmica (Hymenoptera, Sphecidae). Behav Ecol Sociobiol 25:335–348

    Article  Google Scholar 

  • Shine R (1989) Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q Rev Biol 64(4):419–461

    Article  CAS  PubMed  Google Scholar 

  • Shreeves G, Field J (2008) Parental care and sexual size dimorphism in wasps and bees. Behav Ecol Sociobiol 62:843–852

    Article  Google Scholar 

  • Stearns SC (1977) The evolution of life-history traits: a critique of the theory and a review of the data. Annu Rev Ecol Evol Syst 8:145–171

    Article  Google Scholar 

  • Stephens PR, Wiens JJ (2009) Evolution of sexual size dimorphisms in emydid turtles: ecological dimorphism, Rensch’s rule, and sympatric divergence. Evolution 63(4):910–925

    Article  PubMed  Google Scholar 

  • Stillwell RC, Blanckenhorn WU, Teder T, Davidowitz G, Fox CW (2010) Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Annu Rev Entomol 55:227–245

    Article  CAS  PubMed  Google Scholar 

  • Temeles EJ, Pan IL, Brennan JL, Horwitt JN (2000) Evidence for ecological causation of sexual dimorphism in a hummingbird. Science 289(5478):441–443

    Article  CAS  PubMed  Google Scholar 

  • Tormos J, Asis JD, Gayubo SF (1995) Observations on the nesting behaviour of Ammophila laevicollis Andre (Hymenoptera, Sphecidae). Ann Soc Entomol Fr 31:157–163

    Google Scholar 

  • Tornberg R, Mönkkönen M, Pahkala M (1999) Changes in diet and morphology of Finnish goshawks from 1960s to 1990s. Oecologia 121(3):369–376

    Article  Google Scholar 

  • Trumbo ST (2012) Patterns of parental care in invertebrates. In: Royle NJ, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 81–100

    Chapter  Google Scholar 

  • Weaving AJS (1988) Prey selection in several sympatric species of Ammophila W. Kirby (Hymenoptera: Sphecidae) in southern Africa. Ann Cape Prov Mus (Nat Hist) 16:327–349

    Google Scholar 

  • Weaving AJS (1989a) Nesting strategies in some southern African species of Ammophila (Hymenoptera: Sphecidae). J Nat Hist 23:1–16

    Article  Google Scholar 

  • Weaving AJS (1989b) Habitat selection and nest construction behavior in some Afro-tropical species of Ammophila (Hymenoptera, Sphecidae). J Nat Hist 23:847–871. doi:10.1080/00222938900770451

    Article  Google Scholar 

  • Weimerskirch H, Le Corre M, Ropert-Coudert Y, Kato A, Marsac F (2006) Sex-specific foraging behaviour in a seabird with reversed sexual dimorphism: the red-footed booby. Oecologia 146(4):681–691

    Article  PubMed  Google Scholar 

  • Wheeler P, Greenwood PJ (1983) The evolution of reversed sexual dimorphism in birds of prey. Oikos 40(1):145–149

    Article  Google Scholar 

Download references

Acknowledgments

We thank Charlotte Stimmler, who performed some of the measurements, and T. Collett, E. Leadbeater, J. Green, E. Lucas, C. Bridge and the referees for comments on various versions of the manuscript. We also thank J.D. Asis, Y. Barbier, P. Gambino, A.W. Hook, V.L. Kazenas, R.P. Martins, A.S. Menke, M.F. O’Brien, A.M. O’Brien, F.D. Parker, J.A. Rosenheim, V.J. Tepedino and A.J.S. Weaving for kindly giving access to the specimens used in the study.

Conflict of interest

The authors declare that they have no competing interests.

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Author information

Authors and Affiliations

  1. School of Life Sciences, University of Sussex, Falmer, Brighton, BN1 9GQ, UK

    Jeremy Field & James D. J. Gilbert

  2. Department of Medical Oncology, Mount Vernon Hospital, Rickmansworth Road, Northwood, Middlesex, HA6 2RN, UK

    Gavin Shreeves

  3. Allan Wilson Centre, Department of Zoology, University of Otago, P.O. Box 56, Dunedin, 9054, New Zealand

    Martyn Kennedy

  4. Department of Earth Sciences, Natural History Museum, London, SW7 5BD, UK

    Selina Brace

  5. Department of Biological, Biomedical and Environmental Science, University of Hull, Hull, HU6 7RX, UK

    James D. J. Gilbert

Authors
  1. Jeremy Field
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gavin Shreeves
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martyn Kennedy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Selina Brace
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. James D. J. Gilbert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jeremy Field.

Additional information

Communicated by S. Sakaluk

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Field, J., Shreeves, G., Kennedy, M. et al. Sex-biased parental care and sexual size dimorphism in a provisioning arthropod. Behav Ecol Sociobiol 69, 1897–1906 (2015). https://doi.org/10.1007/s00265-015-2002-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-015-2002-1

Keywords

Search

Navigation