Impact of cryptic female choice on insemination success: Larger sized and longer copulating male squid ejaculate more, but females influence insemination success by removing spermatangia

Abstract

In polyandrous mating systems, sperm competition and cryptic female choice (CFC) are well recognized as postcopulatory evolutionary forces. However, it remains challenging to separate CFC from sperm competition and to estimate how much CFC influences insemination success because those processes usually occur inside the female's body. The Japanese pygmy squid, Idiosepius paradoxus, is an ideal species in which to separate CFC from sperm competition because sperm transfer by the male and sperm displacement by the female can be observed directly at an external location on the female's body. Here, we counted the number of spermatangia transferred to, removed from, and remaining on the female body during single copulation episodes. We measured behavioral and morphological characteristics of the male, such as duration of copulation and body size. Although males with larger body size and longer copulation time were capable of transferring larger amounts of sperm, females preferentially eliminated sperm from males with larger body size and shorter copulation time by spermatangia removal; thus, CFC could attenuate sperm precedence by larger males, whereas it reinforces sperm precedence by males with longer copulation time. Genetic paternity analysis revealed that fertilisation success for each male was correlated with remaining sperm volume that is adjusted by females after copulation.

High levels of polyandry, but limited evidence for multiple paternity, in wild populations of the western rock lobster (Panulirus cygnus)

“…The occurrence of cryptic female choice is often more difficult to infer due to the diversity of possible underlying mechanisms and their interactions with sperm competition (reviewed by Firman, Gasparini, Manier, & Pizzari, ). Consequently, evidence of cryptic female choice in decapods is limited, but compelling examples of the phenomenon come from studies of other marine species with external sperm deposition (e.g., Japanese pygmy squid, Idiosepius paradoxus ; Sato, Yoshida, & Kasugai, ) and external fertilization (ocellated wrasse, Symphodus ocellatus ; Alonzo, Stiver, & Marsh‐Rollo, ). Cryptic female choice has been proposed in decapods based on behavioral observations, including failed copulations (Bauer, ; Diesel, ; Ra'anan & Sagi, ) and delayed oviposition (Thiel & Hinojosa, ).…”

Digest: Female squid influence insemination success after mating to show a preference for smaller males*

“…Sato et al (2016) suggest that female preference for small male body size and long ejaculation duration demonstrate CFC and not sperm competition because they are female-driven choices. However, Sato et al (2016) found that CFC did not strongly influence final male paternity, suggesting that while females may bias the spermatangia of some males, male-driven sperm competition may still play a role in this system. Sato et al conclude that female preference for small males may have arisen in the Japanese pygmy squid to counter the large volume of spermatozoa produced by large males.…”

“…The team found that female squid preferentially removed the spermatangia of larger males who copulated quickly-a surprising result after a previous study found that females preferentially removed spermatangia from larger males who copulated for a long time (Sato et al 2014b). Sato et al (2016) suggest that female preference for small male body size and long ejaculation duration demonstrate CFC and not sperm competition because they are female-driven choices. However, Sato et al (2016) found that CFC did not strongly influence final male paternity, suggesting that while females may bias the spermatangia of some males, male-driven sperm competition may still play a role in this system.…”

“…the pygmy squid an excellent system for directly observing CFC and its outcomes. Sato et al (2016) combined direct observation of CFC with second male paternity measures to see which male traits females found most attractive and how female choice influenced the insemination success of attractive and unattractive males. The team measured CFC by counting the number of spermatangia placed, removed, and remaining on the female's body after each copulation act.…”

“…A female can remove the spermatangia from her body before spermatozoa transfer by blowing water on them with her siphon, or by removing and eating them. This behavior makes * This article corresponds to Sato, N., Yoshida, M.-a. and Kasugai, T. (2016), Impact of cryptic female choice on insemination success: Larger sized and longer copulating male squid ejaculate more, but females influence insemination success by removing spermatangia.…”