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Journal of Insect Behavior

, Volume 31, Issue 6, pp 629–641 | Cite as

Sexual Behavior of the Desert Locust During Intra- and Inter-Phase Interactions

  • Y. Golov
  • J. Rillich
  • M. Douek
  • A. R. Harari
  • A. AyaliEmail author
Article

Abstract

Mating and reproduction behaviors and strategies are fundamental aspects of an organism’s evolutionary and ecological success. In locusts, intra- as well as inter-phase reproductive interactions among gregarious and solitarious locust populations have a major impact on the locust population dynamics. However, practically all previous work on locust sexual behavior has been limited to the gregarious phase. Here we provide a first detailed description of pre-copulatory behavior of solitarious desert locusts. We compare our findings with those of previous reports of pre-copulatory behavior of gregarious locusts, focusing on the behavioral elements that serve in inter-sex signaling and communication. We also studied inter-phase (mixed pairs) reproductive interactions. Solitarious males were found to invest more in pre-copulatory courtship and signaling compared to their gregarious counterparts; and solitarious females played a more dominant role in the inter-sex communication than gregarious females. The solitarious females were also less likely to demonstrate rejection-related behavioral patterns than gregarious females. As a consequence of the particular characteristic behavior of each phase, the most successful among intra- and inter-phase pairs were gregarious males with solitary females. Least successful were solitary males paired with gregarious females, indicating a strong asymmetry in inter-phase reproductive interactions.

Keywords

Schistocerca gregaria locust density-dependent phase polyphenism sexual behavior reproductive phenotype 

Notes

Acknowledgments

We are grateful to Moshe Guershon for his assistance in the experiments and analysis and for lively discussions. This work was funded by a grant from the Israel Ministry of Agriculture and Rural Development (891-0277-13). The work in its final stage was partially supported by the German Research Council (DFG; Grant RI 2728/2-1).

Supplementary material

10905_2018_9703_Fig7_ESM.png (619 kb)
Supplementary figure 1

The precopulatory behavioral repertoire of the male (left) and female (right) desert locust in the solitary phase (Mean PO: The probability of an element to occur). The pre-mounting and mounting behavioral elements are listed from step 1 to 7 (S1-S7) and color coded according to relevant body part. Behavioral elements that are shared and mutually exhibited by both sexes are presented in italic bold font. (PNG 618 kb)

10905_2018_9703_MOESM1_ESM.tif (964 kb)
High resolution image (TIF 963 kb)
10905_2018_9703_Fig8_ESM.png (269 kb)
Supplementary figure 2

A comparison of the kinematics of the pre-copulatory behavior of solitary and gregarious male locusts; based on a matrix constructed for all transition probabilities (TP) between behavioral elements in each phase (as detailed in the Methods section and following Golov et al. 2018). The color of the circles representing the different behavioral elements corresponds to the color index used in Fig. S1. Arrows represent the direction of a phase-dependent difference of 15% or more in the TP value between two elements, (red- higher in solitary, black-higher in gregarious locusts). (PNG 268 kb)

10905_2018_9703_MOESM2_ESM.tif (352 kb)
High resolution image (TIF 351 kb)
10905_2018_9703_Fig9_ESM.png (223 kb)
Supplementary figure 3

A comparison of the kinematics of the pre-copulatory behavior of solitary and gregarious female locusts; details as in Fig. S2. (PNG 223 kb)

10905_2018_9703_MOESM3_ESM.tif (315 kb)
High resolution image (TIF 315 kb)

References

  1. Amerasinghe FP (1978) Effects of J.H.I and J.H.III on yellowing, sexual activity and pheromone production in allatectomized male Schistocerca gregaria. J Insect Physiol 24:603–611CrossRefGoogle Scholar
  2. Andersson M, Iwasa Y (1996) Sexual selection. Trends Ecol Evol (Amst) 11:53–58CrossRefGoogle Scholar
  3. Ariel G, Ayali A (2015) Locust collective motion and its modeling. PLoS Comput Biol 11:e1004522CrossRefGoogle Scholar
  4. Arthur NJ, Dyer KA (2015) Asymmetrical sexual isolation but no postmating isolation between the closely related species Drosophila suboccidentalis and Drosophila occidentalis. BMC Evol Biol 15:38CrossRefGoogle Scholar
  5. Chapuis M-P, Loiseau A, Michalakis Y et al (2009) Outbreaks, gene flow and effective population size in the migratory locust, Locusta migratoria: a regional-scale comparative survey. Mol Ecol 18:792–800CrossRefGoogle Scholar
  6. Chapuis M-P, Plantamp C, Blondin L, Pagès C, Vassal JM, Lecoq M (2014) Demographic processes shaping genetic variation of the solitarious phase of the desert locust. Mol Ecol 23:1749–1763CrossRefGoogle Scholar
  7. Cullen DA, Cease AJ, Latchininsky AV et al (2017) From molecules to management: mechanisms and consequences of locust phase polyphenism. Advances in Insect Physiology 53:167–285. Academic PressCrossRefGoogle Scholar
  8. Ellis PE (1959) Learning and social aggregation in locust hoppers. Anim Behav 7:91–IN4CrossRefGoogle Scholar
  9. Ellis PE (1963) Changes in the social aggregation of locust hoppers with changes in rearing conditions. Anim Behav 11:152–160CrossRefGoogle Scholar
  10. Ellis PE, Ashall C (1957) Field studies on diurnal behaviour, movement and aggregation in the desert locust (Schistocerca gregaria Forskǻl). Anti-Locust Bull 25:1–94Google Scholar
  11. Ely SO, Mahamat H, Njagi PGN, Bashir MO, el-Amin Sel-T, Hassanali A (2006) Mate location mechanism and phase-related mate preferences in solitarius desert locust, Schistocerca gregaria. J Chem Ecol 32:1057–1069CrossRefGoogle Scholar
  12. Farrow RA (1979) Population dynamics of the australian plague locust, chortoicetes terminifera (walker), in central western new south wales. I. reproduction and migration in relation to weather. Aust J Zool 27:717CrossRefGoogle Scholar
  13. Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7:1325–1330CrossRefGoogle Scholar
  14. Geva N, Guershon M, Orlova M, Ayali A (2010) Memoirs of a locust: density-dependent behavioral change as a model for learning and memory. Neurobiol Learn Mem 93:175–182CrossRefGoogle Scholar
  15. Golov Y, Rillich J, Harari A, Ayali A (2018) Precopulatory behavior and sexual conflict in the desert locust. PeerJ 6:e4356CrossRefGoogle Scholar
  16. Gray DA (2005) Does courtship behavior contribute to species-level reproductive isolation in field crickets? Behav Ecol 16:201–206CrossRefGoogle Scholar
  17. Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol (Amst) 11:92–98CrossRefGoogle Scholar
  18. Hassanali A, Njagi PG, Bashir MO (2005) Chemical ecology of locusts and related acridids. Annu Rev Entomol 50:223–45Google Scholar
  19. Heifetz Y, Voet H, Applebaum SW (1996) Factors affecting behavioral phase transition in the desert locust, Schistocerca gregaria (Forskål)(Orthoptera: Acrididae). J Chem Ecol 22(9):1717–1734Google Scholar
  20. Ibrahim KM (2001) Plague dynamics and population genetics of the desert locust: can turnover during recession maintain population genetic structure? Mol Ecol 10:581–591CrossRefGoogle Scholar
  21. Ibrahim KM, Sourrouille P, Hewitt GM (2000) Are recession populations of the desert locust (Schistocerca gregaria) remnants of past swarms? Mol Ecol 9:783–791CrossRefGoogle Scholar
  22. Inayatullah C, El Bashir S, Hassanali A (1994) Sexual behavior and communication in the desert locust, Schistocerca gregaria (Orthoptera: Acrididae): sex pheromone in solitaria. Environ Entomol 23:1544–1551CrossRefGoogle Scholar
  23. Injeyan HS, Tobe SS (1981) Phase polymorphism in Schistocerca gregaria: reproductive parameters. J Insect Physiol 27:97–102CrossRefGoogle Scholar
  24. Lazar M, Piou C, Doumandji-Mitiche B, Lecoq M (2016) Importance of solitarious desert locust population dynamics: lessons from historical survey data in Algeria. Entomol Exp Appl 161:168–180CrossRefGoogle Scholar
  25. Loher W (1959) Contributions to the study of the sexual behaviour of Schistocerca gregaria forskål (orthoptera: acrididae). P Proc R Soc A, General Entomology 34:49–56Google Scholar
  26. Loher W (1961) The chemical acceleration of the maturation process and its hormonal control in the male of the desert locust. Proc R Soc B Biol Sci 153:380–397Google Scholar
  27. Maeno KO, Ould Ely S, Nakamura S, Abdellaoui K, Cissé S, Jaavar MEH, Ould Mohamed S’A, Atheimine M, Ould Babah MA (2016) Daily microhabitat shifting of solitarious-phase Desert locust adults: implications for meaningful population monitoring. Springerplus 5:107CrossRefGoogle Scholar
  28. Mahamat H, Hassanali A, Odongo H, Torto B, el-Bashir ES (1993) Studies on the maturation-accelerating pheromone of the desert locust Schistocerca gregaria (Orthoptera: Acrididae). Chemoecology 4:159–164CrossRefGoogle Scholar
  29. Masta SE, Maddison WP (2002) Sexual selection driving diversification in jumping spiders. Proc Natl Acad Sci U S A 99:4442–4447CrossRefGoogle Scholar
  30. Nishide Y, Tanaka S (2012) Yellowing, morphology and behaviour in sexually mature gynandromorphs of the desert locust Schistocerca gregaria. Physiol Entomol 37:379–383CrossRefGoogle Scholar
  31. Norris MJ (1954) Sexual maturation in the desert locust (Schistocerca gregaria Forskål) with special reference to the effects of grouping. Anti-Locust Bull 18:1–44Google Scholar
  32. Norris MJ (1962) Group effects on the activity and behaviour of adult males of the desert locust (Schistocerca gregaria Forsk.) in relation to sexual maturation. Anim Behav 10:275–291CrossRefGoogle Scholar
  33. Nosil P (2012) Ecological speciation. OUP Oxford, OxfordCrossRefGoogle Scholar
  34. Nosil P, Vines TH, Funk DJ (2005) Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719PubMedGoogle Scholar
  35. Obeng-Ofori D, Torto B, Hassanali A (1993) Evidence for mediation of two releaser pheromones in the aggregation behavior of the gregarious desert locust, Schistocerca gregaria (forskal) (Orthoptera: Acrididae). J Chem Ecol 19:1665–1676CrossRefGoogle Scholar
  36. Oberlin UP (1973) Verhaltensbiologische Studien an der europaeischen Wanderheuschrecke Locusta migratoria L. Entomol Gesell Basel 23:12–23Google Scholar
  37. Otte D (1970) A comparative study of communicative behaviour in grasshoppers. Misc Publ Mus Zool Univ Mich 141:1–168Google Scholar
  38. Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol (Amst) 16:364–371CrossRefGoogle Scholar
  39. Pener MP (1965) On the influence of corpora allata on maturation and sexual behaviour of Schistocerca gregaria. J Zool 147:119–136Google Scholar
  40. Pener MP (1967) Effects of allatectomy and sectioning of the nerves of the corpora allata on oöcyte growth, male sexual behaviour, and colour change in adults of Schistocerca gregaria. J Insect Physiol 13:665–684CrossRefGoogle Scholar
  41. Pener MP (1976) The differential effect of the corpora allata on male sexual behaviour in crowded and isolated Locusta migratoria migratorioides (R & F.) males. Acrida 5:189–206Google Scholar
  42. Pener MP, Simpson SJ (2009) Locust phase polyphenism: an update. Advances in Insect Physiology 36:1–272. ElsevierCrossRefGoogle Scholar
  43. Popov GB (1958) Ecological studies on oviposition by swarms of the desert locust (Schistocerca gregaria Forskål) in Eastern Africa. Anti-Locust Bull 31:1–70Google Scholar
  44. Ramirez-Romero R, Garibay-Benítez D, Vargas-Ponce O, Joyce A, Bernal JS (2017) Do assortative mating and immigrant inviability help maintain population genetic structuring of an herbivore on a crop and a wild relative? Insect Sci.  https://doi.org/10.1111/1744-7917.12509
  45. Rhen T, Crews D (2002) Variation in reproductive behaviour within a sex: neural systems and endocrine activation. J Neuroendocrinol 14:517–531CrossRefGoogle Scholar
  46. Roessingh P, Simpson SJ, James S (1993) Analysis of phase-related changes in behaviour of desert locust nymphs. Proc R So Lond B 252(1333):43–49CrossRefGoogle Scholar
  47. Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352CrossRefGoogle Scholar
  48. Strong L, Amerasinghe FP (1977) Allatectomy and sexual receptivity in females of Schistocerca gregaria. J Insect Physiol 23:131–135CrossRefGoogle Scholar
  49. Tanaka S, Zhu D-H (2003) Phase-related differences in mating strategy of a locust (Orthoptera: Acrididae). Ann Entomol Soc Am 96(4):498–502CrossRefGoogle Scholar
  50. Tanaka S, Maeno K, Ould Mohamed S et al (2010) Upsurges of desert locust populations in Mauritania: body coloration, behavior and morphological characteristics. Appl Entomol Zool (Jpn) 45:641–652CrossRefGoogle Scholar
  51. Topaz CM, D’Orsogna MR, Edelstein-Keshet L, Bernoff AJ (2012) Locust dynamics: behavioral phase change and swarming. PLoS Comput Biol 8:e1002642CrossRefGoogle Scholar
  52. Uvarov BP (1966) Phase polymorphism. Grasshoppers and locusts. Cambridge University Press, Cambridge, pp 332–386Google Scholar
  53. Uvarov B (1977) Grasshoppers and locusts. A handbook of general acridology. In: Behaviour, ecology, biogeography, population dynamics, vol 2. Centre for Overseas Pest Research, LondonGoogle Scholar
  54. Whitman DW (1990) Grasshopper chemical communication. In: Chapman RF, Joern A (eds) Biology of grasshoppers. Wiley, New York, pp 357–391Google Scholar
  55. Wybrandt GB, Andersen SO (2001) Purification and sequence determination of a yellow protein from sexually mature males of the desert locust, Schistocerca gregaria. Insect Biochem Mol Biol 31:1183–1189CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of ZoologyTel Aviv UniversityTel AvivIsrael
  2. 2.Department of EntomologyVolcani CenterBet DaganIsrael

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