Advertisement

New information on the evolution of mating behaviour in Sepsidae (Diptera) and the cost of male copulations in Saltella sphondylii

  • 196 Accesses

  • 10 Citations

Abstract

Here we describe the hitherto unknown details of the highly unusual mating behaviour of Saltella sphondylii—a widely cited model for male longevity costs caused by multiple copulations. When compared to the known mating behaviour of 28 sepsid species, we find five unique behavioural elements based on frame-by-frame analyses of video-recordings. These new behaviours are documented with video clips. We suggest that the male longevity costs could be due to copulation bouts that involve multiple insertions of a comparatively membranous phallus into the female. We compare the phallus of the Saltella sphondylii to those from three other species (Themira putris, Parapaleosepsis plebeia, Sepsis punctum).

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2a–d

References

  1. Ang, Y., Puniamoorthy, N., & Meier, R. (2008). Secondarily reduced foreleg armature in Perochaeta dikowi sp.n. (Diptera: Cyclorrhapha: Sepsidae) due to a novel mounting technique. Systematic Entomology, 33, 552–559.

  2. Blanckenhorn, W. U., Muhlhauser, C., Morf, C., Reusch, T., & Reuter, M. (2000). Female choice, female reluctance to mate and sexual selection on body size in the dung fly Sepsis cynipsea. Ethology, 106(7), 577–593.

  3. Blanckenhorn, W. U., Hosken, D. J., Martin, O. Y., Reim, C., Teuschl, Y., & Ward, P. I. (2002). The costs of copulating in the dung fly Sepsis cynipsea. Behavioral Ecology, 13(3), 353–358.

  4. Blanckenhorn, W. U., Dixon, A. F. G., Fairbairn, D. J., Foellmer, M. W., Gibert, P., van der Linde, K., et al. (2007). Proximate causes of Rensch’s rule: Does sexual size dimorphism in arthropods result from sex differences in development time? The American Naturalist, 169(2), 245–257.

  5. Bowsher, J. H., & Nijhout, H. F. (2007). Evolution of novel abdominal appendages in a sepsid fly from histoblasts, not imaginal discs. Evolution & Development, 9(4), 347–354.

  6. Bowsher, J. H., & Nijhout, H. F. (2009). Partial co-option of the appendage patterning pathway in the development of abdominal appendages in the sepsid fly Themira biloba. Development Genes and Evolution, 219(11–12), 577–587.

  7. Burton-Chellew, M. N., Sykes, E. M., Patterson, S., Shuker, D. M., & West, S. A. (2007). The cost of mating and the relationship between body size and fitness in males of the parasitoid wasp Nasonia vitripennis. Evolutionary Ecology Research, 9, 921–934.

  8. Cordts, R., & Partridge, L. (1996). Courtship reduces longevity of male Drosophila melanogaster. Animal Behavior, 52, 269–278.

  9. Doi, M., Matsuda, M., Tomaru, M., Matsubayashi, H., & Oguma, Y. (2001). A locus for female discrimination behavior causing sexual isolation in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 98(12), 6714–6719.

  10. Eberhard, W. G. (1999). Mating systems of sepsid flies and sexual behavior away from oviposition sites by Sepsis neocynipsea (Diptera: Sepsidae). Journal of the Kansas Entomological Society, 72(1), 129–130.

  11. Eberhard, W. G. (2001a). Courtship and multi-stage transfer of material to the female’s wings during copulation in Microsepsis armillata (Diptera: Sepsidae). Journal of the Kansas Entomological Society, 74(2), 70–78.

  12. Eberhard, W. G. (2001b). Species-specific genitalic copulatory courtship in sepsid flies (Diptera, Sepsidae, Microsepsis) and theories of genitalic evolution. Evolution, 55(1), 93–102.

  13. Eberhard, W. G. (2002a). The function of female resistance behavior: Intromission by male coercion vs. female cooperation in sepsid flies (Diptera: Sepsidae). Revista de Biologia Tropical, 50(2), 485–505.

  14. Eberhard, W. G. (2002b). Physical restraint or stimulation? The function(s) of the modified front legs of male Archisepsis diversiformis (Diptera, Sepsidae). Journal of Insect Behavior, 15(6), 831–850.

  15. Eberhard, W. G. (2002c). The relation between aggressive and sexual behavior and allometry in Palaeosepsis dentatiformis flies (Diptera: Sepsidae). Journal of the Kansas Entomological Society, 75(4), 317–332.

  16. Eberhard, W. G. (2003). Sexual behavior and morphology of Themira minor (Diptera: Sepsidae) males and the evolution of male sternal lobes and genitalic surstyli. Canadian Entomologist, 135(4), 569–581.

  17. Eberhard, W. G. (2005). Sexual morphology of male Sepsis cynipsea (Diptera: Sepsidae): lack of support for lock-and key and sexually antagonistic morphological coevolution hypotheses. Canadian Entomologist, 137, 551–565.

  18. Eberhard, W. G., & Pereira, F. (1996). Functional morphology of male genitalic surstyli in the dungflies Achisepsis diversiformis and A. ecalcarata (Diptera: Sepsidae). Journal of the Kansas Entomological Society, 69(4 SUPPL), 43–60.

  19. Fabricius, J. C. (1794). Entomologia systematica emendata et aucta. Secundum classes, ordines, genera, species adjectis synonymis, locis, observationibus, descriptionibus. Hafniae [= Copenhagen], 4, 1–472.

  20. Ferkau, C., & Fischer, K. (2006). Costs of reproduction in male Bicyclus anynana and Pieris napi butterflies: effects of mating history and food limitation. Ethology, 112, 1117–1127.

  21. Frey, J. E., Bierbaum, T. J., & Bush, G. L. (1992). Differences among sibling species among Rhagoletis mendax and R. pomonella (Diptera, Tephritidae) in their antennal sensitivity to host fruit compounds. Journal of Chemical Ecology, 18(11), 2011–2024.

  22. Hammer, O. (1941). Biological and ecological investigations on flies associated with pasturing cattle and their excrement. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Khobenhavn, 105, 141–394.

  23. Hare, E. E., Peterson, B. K., Iyer, V. N., Meier, R., & Eisen, M. B. (2008). Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation. PLoS Genetics, 4(6), e1000106.

  24. Henry, C. S., Brooks, S. J., Duelli, P., & Johnson, J. B. (2002). Discovering the true Chrysoperla carnea (Insecta: Neuroptera: Chrysopidae) using song analysis, morphology, and ecology. Annals of the Entomological Society of America, 95(2), 172–191.

  25. Ingram, K. K., Laamanen, T., Puniamoorthy, N., & Meier, R. (2008). Lack of morphological coevolution between male forelegs and female wings in Themira (Sepsidae: Diptera: Insecta). Biological Journal of the Linnean Society, 93(2), 227–238.

  26. Kotiaho, J. S., & Simmons, L. W. (2003). Longevity cost of reproduction for males but no longevity cost of mating or courtship for females in the male-dimorphic dung beetle Onthophagus binodis. Journal of Insect Physiology, 49, 817–822.

  27. Laamanen, T. R., Meier, R., Miller, M. A., Hille, A., & Wiegmann, B. M. (2005). Phylogenetic analysis of Themira (Sepsidae: Diptera): sensitivity analysis, alignment, and indel treatment in a multigene study. Cladistics, 21(3), 258–271.

  28. Linnaeus, C. (1758). Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum caracteribus, differentiis, synonymis, locis. Ed. 10. Holmiae [= Stockholm], 1, 824.

  29. Martin, O. Y., & Hosken, D. J. (2002). Strategic ejaculation in the common dung fly Sepsis cynipsea. Animal Behavior, 63(3), 541–546.

  30. Martin, O. Y., & Hosken, D. J. (2004). Copulation reduces male but not female longevity in Saltella sphondylli (Diptera: Sepsidae). Journal of Evolutionary Biology, 17, 357–362.

  31. Meier, R. (1995a). Cladistic analysis of the Sepsidae (Cyclorrhapha: Diptera) based on a comparative scanning electron microscope study of larvae. Systematic Entomology, 20(2), 99–128.

  32. Meier, R. (1995b). A comparative SEM study of the eggs of the Sepsidae (Diptera) with a cladistic analysis based on egg, larval and adult characters. Insect Systematics & Evolution, 26(4), 425–438.

  33. Meier, R. (1996). Larval morphology of the Sepsidae (Diptera: Sciomyzoidea), with a cladistic analysis using adult and larval characters. Bulletin of the American Museum of Natural History, 228, 3–147.

  34. Meier, R. (1997). A test and review of the empirical performance of the ontogenetic criterion. Systematic Biology, 46(4), 699–721.

  35. de Meijere, J. C. H. (1906). Über einige indo-australische Dipteren des Ungarischen National- Museums, bez. des Naturhistorischen Museums zu Genua. Annales Historico-Naturales Musei Nationalis Hungarici, 4, 165–196.

  36. de Meijere, J. C. H. (1913). H. Sauter’s Formosa Ausbeute. Sepsinae. (Dipt.). Annales Historico-Naturales Musei Nationalis Hungarici, 11, 114–124.

  37. Melander, A. L., & Spuler, A. (1917). The Dipterous families Sepsidae and Piophilidae. Bulletin of the Washington Agricultural Experimental Station, 143, 1–103.

  38. Muhlhauser, C., & Blanckenhorn, W. U. (2002). The costs of avoiding matings in the dung fly Sepsis cynipsea. Behavioral Ecology, 13(3), 359–365.

  39. Muhlhauser, C., & Blanckenhorn, W. U. (2004). The quantitative genetics of sexual selection in the dung fly Sepsis cynipsea. Behaviour, 141(Part 3), 327–341.

  40. Oliver, C., & Cordero, C. (2009). Multiple mating reduces male survivorship but not ejaculate size in the polygamous insect Stenomacra marginella (Heteroptera: Largidae). Evolutionary Ecology, 23, 417–424.

  41. Ozerov, A. L. (2005). World catalogue of the family Sepsidae (Insecta: Diptera). Zoologicheskie issledovania (Zool. Stud.), 8, 1–74.

  42. Parker, G. A. (1972a). Reproductive behaviour of Sepsis cynipsea (L.) (Diptera: Sepsidae) I. A preliminary analysis of the reproductive strategy and its associated behaviour patterns. Behaviour, 41, 172–206.

  43. Parker, G. A. (1972b). Reproductive behaviour of Sepsis cynipsea (L.) (Diptera: Sepsidae) II. The significance of the precopulatory passive phase and emigration. Behaviour, 41, 242–250.

  44. Paukku, S., & Kotiaho, J. S. (2005). Cost of reproduction in Callosobruchus maculatus: Effects of mating on male longevity and the effect of male mating status on female longevity. Journal of Insect Physiology, 51, 1220–1226.

  45. Pont, A. C., & Meier, R. (2002). The Sepsidae (Diptera) of Europe. Fauna Entomologica Scandinavica, 37, 1–221.

  46. Prowse, N., & Partridge, L. (1997). The effects of reproduction on longevity and fertility in male Drosophila melanogaster. Journal of Insect Physiology, 43, 501–512.

  47. Puniamoorthy, N., Su, K. F. Y., & Meier, R. (2008). Bending for love: losses and gains of sexual dimorphisms are strictly correlated with changes in the mounting position of sepsid flies (Sepsidae: Diptera). BMC Evolutionary Biology, 8, 155.

  48. Puniamoorthy, N., Ismail, M. R. B., Tan, D. S. H., & Meier, R. (2009). From kissing to belly stridulation: comparative analysis reveals surprising diversity, rapid evolution, and much homoplasy in the mating behaviour of 27 species of sepsid flies (Diptera: Sepsidae). Journal of Evolutionary Biology, 22, 2146–2156.

  49. Puniamoorthy, N., Kotrba, M., & Meier, R. (2010). Unlocking the “black box”: internal female genitalia in Sepsidae (Diptera) evolve fast and are species-specific. BMC Evolutionary Biology, 10, 275.

  50. Schrank, F. de P., (1803). Fauna boica. Durchgedachte Geschichte der in Baiern einheimischen und zahmen Tiere, Landshut, 3(1), 1–272.

  51. Schulze, K. S. (1999). The evolution of mating systems in black scavenger flies (Diptera: Sepsidae). PhD thesis. University of Arizona.

  52. South, S. H., Steiner, D., & Arnqvist, G. (2009). Male mating costs in a polygynous mosquito with ornaments expressed in both sexes. Proceedings of the Royal Society of London B, 276, 3671–3678.

  53. Su, K. F. Y., Kutty, S., & Meier, R. (2008). Morphology versus Molecules: The phylogenetic relationships of Sepsidae (Diptera: Cyclorrhapha) based on morphology and DNA sequence data from ten genes. Cladistics, 24, 902–916.

  54. Tan, D. S. H., Ang, Y., Lim, G. S., Ismail, M. R., & Meier, R. (2010). From ‘cryptic species’ to integrative taxonomy: an iterative process involving DNA sequences, morphology, and behaviour leads to the resurrection of Sepsis pyrrhosoma (Sepsidae: Diptera). Zoologica Scripta, 39, 51–61.

  55. Ward, P. I., Hemmi, J., & Roosli, T. (1992). Sexual conflict in the dung fly Sepsis cynipsea. Functional Ecology, 6(6), 649–653.

Download references

Acknowledgements

We would like to thank all members of the Evolutionary Biology Lab, especially Martin Chew for his assistance in generating the molecular phylogeny, and Nalini Puniamoorthy for her helpful comments for the manuscript. This study was financially supported by grant R154-000-476-112 from the Ministry of Education in Singapore.

Author information

Correspondence to Rudolf Meier.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(MPG 7602 kb)

 (MPG 21198 kb)

 (MPG 9142 kb)

ESM 1

(MPG 7602 kb)

ESM 2

 (MPG 21198 kb)

ESM 3

 (MPG 9142 kb)

Appendix

Appendix

Character descriptions modified from Puniamoorthy et al. (2009)

  1. (1)

    ‘Circling’—0: Absent (Male approach without gliding motion); 1: Present (Male circling female in a gliding motion, head and thorax leading the change of direction with abdomen bent at an angle)

  2. (2)

    Initial mount—0: Male jumps or climbs onto female; 1: Male bends abdomen anteriad to establish direct genital contact

  3. (3)

    Effect of struggle on in-copula position of pair—0: Females do not flip over; 1: Pair flipping over resulting in male on his back and female with her legs in air)

  4. (4)

    Male proboscis–female interaction—0: No contact between male proboscis and female; 1: Male extends proboscis to ‘kiss’ female ocelli; 2: Male extends proboscis to tap dorsal part of female thorax

  5. (5)

    Male grasp of female wingbase—0: Forelegs resting on female thorax; 1: Forelegs release wingbase only at separation; 2: Forelegs release female wings well before separation

  6. (6)

    Male foreleg after release—0: Resting against female thorax (no movement); 1: Male foreleg interacting with female thorax and, or foreleg

  7. (7)

    Midleg position—0: Male midlegs always in contact with female; 1: Male mid legs are stretched out away from female body i.e. ‘balancing’ (for extended period); 2: Male midlegs are not stretched out and are not in contact with female

  8. (8)

    Motion restricted to mid tarsus—0: No independent tarsal movements; 1: Curling (movement of the tarsi 2–4 against the barsitarsus); 2: Quiver (vibration of entire tarsus without movement of tibia or femur)

  9. (9)

    Non-contact midleg movement—0: Simultaneous usage of both midlegs; 1: Simultaneous and alternate; 2: Alternate usage of both midlegs

  10. (10)

    Direction of midleg movement—0: Male midleg stretched out and stationary; 1: Male midleg towards female eye; 2: Male midlegs move posteriad

  11. (11)

    Male midleg movement away from female head—0: Smooth return without any interruptions; 1: Return interrupted by midleg waves

  12. (12)

    Midleg rotation during tarsal curl—0: Midleg curling in a horizontal plane; 1: Curling direction shifting from horizontal to vertical plane through leg rotation; 2: Curling in a vertical plane

  13. (13)

    Number of tarsal curls per midleg movement—0: Single curl per midleg movement; 1: Multiple curls

  14. (14)

    Midleg interaction with female head—0: No with contact female head; 1: Male uses his mid tarsi to rub head; 2: Male uses his mid tarsi to tap head (singular movements)

  15. (15)

    Midleg interaction with female abdomen—0: No with contact female abdomen; 1: Male uses his midlegs to tap female abdomen

  16. (16)

    Midleg interaction with female thorax—0: Absent; 1: Midlegs tap lateral surface (singular movements); 2: Midlegs ‘stroke’ lateral surface (extended rubbing); 3: Midlegs ‘stroke’ dorsal surface (extended rubbing)

  17. (17)

    Female wings bent down by male midlegs—0: Male midlegs rest on female wings; 1: Male midlegs used to forcibly bend down female wings

  18. (18)

    Midleg to midleg grasp—0: Male midlegs not holding female mid legs; 1: Male uses midlegs to hold onto female midlegs

  19. (19)

    Contact of male hindleg with substrate—0: Hindleg not in contact with substrate when female moves; 1: Mounted male’s hindleg is dragged along substrate when female moves; 2: Mounted male walks in tandem with female instead of being dragged

  20. (20)

    Non-contact movement of male hindlegs—0: Absent; 1: Hindlegs curl backwards 360° like a backward ‘butterfly stroke’; 2: ‘Cycling’ ( i.e. like a peddling motion); 3: Curling (Hindlegs stretched out and vibration of the 2–4 tarsal segments against the barsitarsus)

  21. (21)

    Usage of hindlegs—0: No direct contact with female; 1: Tap ventral side of female abdomen; 2: Rub repeatedly on dorsal side of female wing; 3: Rub repeatedly wing margin

  22. (22)

    Midleg–hindleg rub—0: No contact between male mid and hindlegs; 1: Males rub their hindlegs with their midlegs

  23. (23)

    Part of female body male rubs after rubbing his hindlegs—0: Wing; 1: Thorax; 2: Head; 3: Abdomen; 4: Midlegs

  24. (24)

    Movement of male abdomen—0: Abdomen maintained horizontally without any movement; 1: Abdomen lifted >90° over the thorax when mounted on female; 2: Male shakes abdomen vigorously from side to side (prior to mounting)

  25. (25)

    Surstylus stimulation prior to genital contact—0: Males only lower abdomen to establish genital contact; 1: Male repeatedly lowers abdomen to stimulate female using the surstylis, either by vibration or by tapping on dorsal surface of female abdomen; 2: Male repeatedly lowers surstylus to stimulate female close to her genital opening; 3: Male lowers surstylus to stimulate on ventral surface of female abdomen

  26. (26)

    Male tapping female with modified fourth sternites—0: Modified 4th sternites of males used to tap or stroke dorsal part of female abdomen; 1: Ventral part of female abdomen

  27. (27)

    Separation after copulation—0: Quick (one or two 180° turns by the male); 1: Long (involving a prolonged struggle between male and female in trying to break genital contact); 2: Quick but not involving turns by the male

  28. (28)

    Female Shake—0: Absent (no violent side to side movement); 1: Present

  29. (29)

    Type of female shake—0: Horizontally; 1: Vertically

  30. (30)

    Female foreleg movements—0: No significant movements of forelegs; 1: Female intermittently lifts forelegs off the substrate; 2: Female repeatedly lifts forelegs above head

  31. (31)

    Female hindleg movements—0: Female hindlegs not used to interact with male; 1: Female hindleg used to ‘kick’ male; 2: Female hindleg ‘rubbing’ male hindlegs

  32. (32)

    Female ejection of ovipositor when male is mounted—0: Absent; 1: Female ejects ovipositor when after genital contact; 2: Female ejects ovipositor prior to genital contact

  33. (33)

    Use of male midleg—0: No forceful contact with female head; 1: Male uses midleg to ‘beat’ female head

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Tan, D.S.H., Ng, S.R. & Meier, R. New information on the evolution of mating behaviour in Sepsidae (Diptera) and the cost of male copulations in Saltella sphondylii . Org Divers Evol 11, 253 (2011). https://doi.org/10.1007/s13127-011-0054-2

Download citation

Keywords

  • Sepsidae
  • Mating cost
  • Mating behaviour
  • Longevity
  • Polyandry
  • Sexual conflict