Temporal shift between daily sperm movement and mating (sperm reflux) in the Asian comma butterfly, Polygonia c-aureum

Authors: HIROYOSHI, SATOSHI - Tokyo University Of Agriculture & Technology; MITSUNAGA, TAKAYUKI - National Agriculture And Food Research Organization (NARO), Agricultrual Research Center; Reddy, Gadi V.P.

Submitted to: Entomologia Experimentalis et Applicata
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/15/2020
Publication Date: 10/9/2020
Citation: Hiroyoshi, S., Mitsunaga, T., Reddy, G.V. 2020. Temporal shift between daily sperm movement and mating (sperm reflux) in the Asian comma butterfly, Polygonia c-aureum L. (Lepidoptera: Nymphalidae). Entomologia Experimentalis et Applicata. 168(11):857-868. https://doi.org/10.1111/EEA.12980.
DOI: https://doi.org/10.1111/EEA.12980

Interpretive Summary: In Lepidoptera, the sperm produced in the testis migrate into the vasa deferentia via the vasa efferentia and from the vasa deferentia to the duplex in a daily rhythm. This topic was presented for the first time, because sperm reflux is poorly understood in all animals including insects. Our results suggest that the temporal rhythm of eupyrene sperm movement is different from that of mating (sperm reflux). For this reason, the daily pattern of sperm movement would not disrupt sperm reflux specific at mating. Sperm reflux stops at the middle portion of the vasa deferentia. This may be related to the fact that the peristatic movement of upper vasa deferentia from up (testis side) to down (vas deferens side) occurs all day. Even if sperm movement from the testis to the upper vasa deferentia occurs during mating, it does not disrupt the sperm reflux occurring between the middle vasa deferentia and the duplex. Although apyrene sperm did not show distinct daily rhythm, this seems likely to be related to the abundance of apyrene sperm in comparison with eupyrene sperm and that apyrene sperm are free in post-testicular organs, having no need of complicated morphological changes. In conclusion, the temporal shift between daily eupyrene sperm movement and sperm reflux would be useful in performing multiple matings following ejaculation of sufficient numbers of sperm in nymphalid butterfly.

Technical Abstract: Abstract: Temporal changes in mating behavior and daily sperm movement were examined in adult males of a nymphalid butterfly, Polygonia c-aureum L. (Lepidoptera: Nymphalidae), reared under an L15:D9 photoperiod at 21'. In this butterfly, when extra sperm are present in the duplex at mating, sperm reflux occurs: extra sperm are moved from the duplex to the lower and middle portions of the vasa deferentia by peristatic movement of the lower portion of vasa deferentia. On the other hand, it is known in several moth species that daily sperm movement from the testis to the upper portion of the vasa deferentia and from the upper vasa deferentia to the duplex occurs in a circadian manner. If sperm reflux and daily sperm movement occur at the same time, it could create confusion, because these sperm movements are oppositely directed to each other. Our results showed that most matings occurred during the second half of photophase, whereas daily eupyrene sperm movement from the upper to the middle portion of the vasa deferentia occurred immediately after light on (early photophase), indicating the presence of a time lag between mating and daily sperm movement. As sperm reflux occurs during mating, these two oppositely directed sperm movements could be performed without conflict.