Mating behaviour and its relationship with morphological features in the millipede Pachyiulus hungaricus (Karsch, 1881) (Myriapoda, Diplopoda, Julida)

Mating behaviour and its relationship with morphological features in the millipede Pachyiulus hungaricus (Karsch, 1881) (Myriapoda, Diplopoda, Julida)

Although millipedes (Diplopoda) represent one of the most diverse classes of arthropods, data concerning details of theirmating behaviour are very scarce. In this work, we explored mating behaviour of the European millipedePachyiulus hungaricusunderlaboratory conditions, and its relationship with the size and shape of certain morphological traits. We conducted 3 types of behaviouraltests: a mating arena test, a female choice test, and a male choice test. Premating behaviour wassequencedin 5 behavioural stepsand, together with the duration of copulation, scored in all mating assays. Males were the more active sex in searching for mates, whilefemales were the choosier sex. Furthermore, in the choice tests, previous mating partners had significantly more copulations than newones, thus raising questions about postcopulatory sexual selection in this species. On the other hand, our results indicate that size and/orshape of the tested morphological traits, except for the shape of the male walking legs, were not subject to precopulatory sexual selection.Other sensory domains known to influence courtship behaviour need to be investigated in this regard inP. hungaricus.

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  • Abràmoff MD, Magalhães PJ, Ram SJ (2004). Image processing with ImageJ. Biophotonics International 11: 36-42.
  • Adolph SC, Geber MA (1995). Mate guarding, mating success and body size in the tropical millipede Nyssodesmus python (Peters) (Polydesmida: Platyrhacidae). Southwest Nat 40: 56-61.
  • Andrés JA, Cordero Rivera A (2000). Copulation duration and fertilization success in a damselfly: an example of cryptic female choice? Anim Behav 59: 695-703.
  • Arnqvist G, Rowe L (1995). Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proc R Soc Lond B Biol Sci 261: 123-127.
  • Arnqvist G, Danielsson I (1999a). Postmating sexual selection: the effects of male body size and recovery period on paternity and egg production rate in a water strider. Behav Ecol 10: 358-365.
  • Arnqvist G, Danielsson I (1999b). Copulatory behavior, genital morphology, and male fertilization success in water striders. Evolution 53: 147-156.
  • Barnett M, Telford SR, De Villiers CJ (1993). Sperm displacement in a millipede? An investigation into the genital morphology of the southern African spirostreptid millipede Orthoporus pyrhocephalus . J Zool 231: 511-522.
  • Baena ML, Macías-Ordó ñ ez R (2015). Mobility and mating frequency in the scramble competition polygyny of a chrysomelid beetle. Behav Ecol 26: 416-424.
  • Barnett M, Telford SR (1994). The timing of insemination and its implications for sperm competition in a millipede with prolonged copulation. Anim Behav 48: 482-484.
  • Barnett M, Telford SR, Tibbies BJ (1995). Female mediation of sperm competition in the millipede Alloporus uncinatus (Diplopoda: Spirostreptidae). Behav Ecol Sociobiol 36: 413-419.
  • Blower JG (1985). Millipedes. In: Kermack DM, Barnes RSK, editors. Linnean Society Synopses of the British Fauna (New Series), No 35. London, UK: E. J. Brill/Dr. W. Backhuys.
  • Burns M (2005). The role of size and defensive compounds in mate choice by Nyssodesmus python (Polydesmida: Platyrhacidae). Report. Tampa, FL, USA: University of South Florida. http:// digital.lib.usf.edu/SFS0001374/00001.
  • Carey CJ, Bull CM (1986). Recognition of mates in the Portuguese millipede Ommatoiulus moreletii. Austr J Zool 34: 837-842.
  • Cator LJ, Zanti Z (2016). Size, sounds and sex: interactions between body size and harmonic convergence signals determine mating success in Aedes aegypti. Parasite Vectors . doi: 10.1186/s13071- 016-1914-6.
  • Cooper MI, Telford SR (2000). Copulatory sequences and sexual struggles in millipedes. J Insect Behav 13: 217-230.
  • Davies NB (1991). Mating systems. In: Krebs JR, Davies NB, editors. Behavioural Ecology: An Evolutionary Approach. 3rd ed. Oxford, UK: Blackwell Scientific Publications, pp. 263-294.
  • Drake AG, Klingenberg CP (2008). The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc R Soc Lond B Biol Sci 275: 71-76.
  • Dugatkin LA (2004). Principles of Animal Behavior. 1st ed. New York, NY, USA: WW Norton & Company, Inc.
  • Eberhard WG (1985). Sexual Selection and Animal Genitalia. Cambridge, MA, USA: Harvard University Press.
  • Eberhard WG (1996). Female Control: Sexual Selection by Cryptic Female Choice. Princeton, NJ, USA: Princeton University Press.
  • Haacker U (1969). An attractive secretion in the mating behaviour of a millipede. Z Tierpsychol 26: 988-990.
  • Hagler JR, Jackson CG (2001). Methods for marking insects: current techniques and future prospects. Annu Rev Entomol 46: 511- 543.
  • Harari AR, Landolt PJ, O’Brien CW, Brockmann HJ (2003). Prolonged mate guarding and sperm competition in the weevil Diaprepes abbreviatus (L.). Behav Ecol 14: 89-96.
  • Helinski MEH, Harrington LC (2011). Male mating history and body size influence female fecundity and longevity of the dengue vector Aedes aegypti . J Med Entomol 48: 202-211.
  • Holwell GI, Allen PJD, Goudie F, Duckett PE, Painting CJ (2016). Male density influences mate searching speed and copulation duration in millipedes (Polydesmida: Gigantowales chisholmi ). Behav Ecol Sociobiol 70: 1381-1388.
  • Hopkin SP, Read HJ (1992). The Biology of Millipedes. Oxford, UK: Oxford University Press.
  • Ilić BS, Mitić BM, Makarov SE (2016). Sexual dimorphism in Apfelbeckia insculpta (L. Koch, 1867) (Myriapoda: Diplopoda: Callipodida). Arch Biol Sci: doi:10.2298/ABS160229060I.
  • Jojić V, Nenadović J, Blagojević J, Paunović M, Cvetković D, Vujošević M (2012). Phenetic relationships among four Apodemus species (Rodentia, Muridae) inferred from skull variation. Zool Anz 251: 26-37.
  • Jones TM, McNamara KB, Colvin PGR, Featherston R, Elgar MA (2006). Mating frequency, fecundity and fertilization success in the hide beetle, Dermestes maculatus . J Insect Behav 19: 357- 371.
  • Kawano K (2000). Genera and allometry in the stag beetle family Lucanidae, Coleoptera. Ann Entomol Soc Am 93: 198-207.
  • Klingenberg CP (2011). MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11: 353-357.
  • Koch M (2015). Diplopoda: general morphology. In: Minelli A, editor. The Myriapoda. Vol. 2. Leiden, the Netherlands: Brill, pp. 7-67.
  • Lazić MM, Carretero MA, Crnobrnja-Isailović J, Kaliontzopoulou A (2015). Effects of environmental disturbance on phenotypic variation: an integrated assessment of canalization, developmental stability, modularity, and allometry in lizard head shape. Am Nat 185: 44-58.
  • Lewis SM, Austad SN (1990). Sources of intraspecific variation in sperm precedence in red flour beetles. Am Nat 135: 351-359.
  • Lewis SM, Austad SN (1994). Sexual selection in flour beetles: the relationship between sperm precedence and male olfactory attractiveness. Behav Ecol 5: 219-224.
  • Li YY, Yu JF, Lu Q, Xu J, Ye H (2014). Female and male moths display different reproductive behavior when facing new versus previous mates. Plos One 9: e109564.
  • Lu W, Wang Q, Tian M, Xu J, Lv J, Qin A (2013). Mating behavior and sexual selection in a polygamous beetle. Curr Zool 59: 257-264.
  • Machado G, Requena GS, Gadea CT, Stanley E, Macías-Ordóñez R (2015). Male and female mate choice in harvestmen: general patterns and inferences on the underlying processes. In: Peretti AV, Aisenberg A, editors. Cryptic Female Choice in Arthropods: Patterns, Mechanisms and Prospects. Cham, Switzerland: Springer, International Publishing, pp. 169-201.
  • Makarov SE, Ćurčić BPM, Tomić VT, Legakis A (2004). The Diplopods of Serbia, Montenegro and the Republic of Macedonia. Monographs, Volume IX. Institute of Zoology- Faculty of Biology, University of Belgrade; Hellenic Zoological Society, Committee for Karst and Speleology–Serbian Academy of Sciences and Arts: Belgrade–Athens.
  • Mathews PL, Bultman TL (1993). Mating behaviour of a parajulid millipede, Aniulus bollmani. Can J Zool 71: 2297-2300.
  • Mauriès, JP (1969). Observations sur la biologie (sexualité, périodomorphose) de Typhloblaniulus lorifer consoranensis Brölemann (Diplopoda, Blaniulidae). Ann Spéléol 24: 495 - 504.
  • Minelli A, Michalik P (2015). Diplopoda: reproduction. In: Minelli A, editor. The Myriapoda. Vol. 2. Leiden, the Netherlands: Brill, pp. 237-265.
  • Moczek AP, Emlen DJ (1999). Proximate determination of male horn dimorphism in the beetle Onthophagus taurus (Coleoptera: Scarabaeidae). J Evol Biol 12: 27-37.
  • Okada Y, Hasegawa E (2005) Size-dependent precopulatory behavior as mate-securing tactic in the Japanese stag beetle, Prosopocoilus inclinatus (Coleoptera; Lucanidae). J Ethol 23: 99-102.
  • Pavković-Lučić S, Kekić V, Čvoro A (2009). Larger male mating advantage depends on sex ratio in Drosophila melanogaster. Ethol Ecol Evol 21: 155-160.
  • Puniamoorthy N, Blackenhorn WU, Schäfer MA (2012). Differential investment in pre- vs. post-copulatory sexual selection reinforces a cross-continental reversal of sexual size dimorphism in Sepsis punctum (Diptera: Sepsidae). J Evolution Biol 25: 2253-2263.
  • Rohlf FJ (2008). TpsDig, Version 2.12. Stony Brook, NY, USA: SUNY at Stony Brook. http://life.bio.sunysb.edu/morph/soft-dataacq. html.
  • Rowe M (2010). Copulation, mating system and sexual dimorphism in an Australian millipede, Cladethosoma clarum. Aust J Zool 58: 127-132.
  • Sierwald P, Bond JE (2007). Current status of the myriapod class Diplopoda (millipedes): taxonomic diversity and phylogeny. Annu Rev Entomol 52: 401-420.
  • Simmons LW, Parker GA (1992). Individual variation in sperm competition success of yellow dung flies Scatophaga stercoraria. Evolution 46: 366-375.
  • Simmons LW, Stockley P, Jackson RL, Parker GA (1996). Sperm competition or sperm selection: no evidence for female influence over paternity in yellow dung flies Scatophaga stercoraria . Behav Ecol Sociobiol 38: 199-206.
  • Sheets HD (2003). IMP: Integrated Morphometrics Package. Buffalo, NY, USA: Department of Physics, Canisius College. http:// www3.canisius.edu/~sheets/morphsoft.html.
  • Sherratt E, Klingenberg CP, Wilkinson M, Gower DJ (2014). Evolution of cranial shape in caecilians (Amphibia: Gymnophiona). Evol Biol 41: 528-545.
  • Shuster S, Wade M (2003). Mating Systems and Strategies. Princeton, NJ, USA: Princeton University Press.
  • Tadler A (1993). Genitalia fitting, mating-behavior and possible hybridization in millipedes of the genus Craspedosoma (Diplopoda, Chordeumatida, Craspedosomatidae). Acta Zool 74: 215-225.
  • Tadler A (1996). Functional morphology of genitalia of four species of julidan millipedes (Diplopoda: Nemasomatidae: Julidae). Zool J Linn Soc 118: 83-97.
  • Tanabe T, Sota T (2008). Complex copulatory behavior and the proximate effect of genital and body size differences on mechanical reproductive isolation in the millipede genus Parafontaria . Am Nat 171: 692-699.
  • Telford SR, Dangerfield JM (1990). Manipulation of the sex ratio and duration of copulation in the tropical millipede Alloporus uncinatus : a test of the copulatory guarding hypothesis. Anim Behav 40: 984-986.
  • Telford SR, Dangerfield JM (1993a). Mating tactics in the tropical millipede Alloporus uncinatus (Diplopoda: Spirostreptidae). Behaviour 124: 45-56.
  • Telford SR, Dangerfield JM (1993b). Mating behavior and mate choice experiments in some tropical millipedes (Diplopoda: Spirostreptidae). S Afr J Zool 28: 155-160.
  • Terzić T, Anđelković M, Stamenković-Radak M (1994). Effect of fluorescent dust, as a marker, on the frequency of mating in Drosophila melanogaster . Dros Inf Serv 75: 164-165.
  • Wedell N (1991). Sperm competition selects for nuptial feeding in a bushcricket. Evolution 45: 1975-1978.
  • Wenninger EJ, Averill AL (2006). Influence of body and genital morphology on relative male fertilization success in oriental beetle. Behav Ecol 17: 656-663.
  • Wilson HM, Anderson LI (2004). Morphology and taxonomy of Paleozoic millipedes (Diplopoda: Chilobognatha: Archipolypoda) from Scotland. J Paleontol 78: 169-184.
  • Wojcieszek JM, Simmons LW (2011). Male genital morphology influences paternity success in the millipede Antichiropus variabilis . Behav Ecol Sociobiol 65: 1843-1856.
  • Wongthamwanich N, Panha S, Sitthicharoenchai D, Pradatsundarasar A, Seelanan T, Enghoff H, Thirakhupt K (2012). Daily activities of the giant pill-millipede Zephronia cf. viridescens Attems, 1936 (Diplopoda: Sphaerotheriida: Zephroniidae) in a deciduous forest in northern Thailand. Zool Stud 51: 913-926.
  • Yang LH, Wang Q (2004). Premating sexual selection in Nysius huttoni White (Heteroptera: Lygaeidae) in relation to morphometric traits. J Insect Behav 17: 695-707.
  • Zeh JA, Newcomer SD, Zeh DW (1998). Polyandrous females discriminate against previous mates. P Natl Acad Sci USA 95: 13732-13736.