Context-dependent behavioural plasticity compromises disruptive selection of sperm traits in squid

Abstract

Sperm morphology is generally uniform within a species due to selective pressures that act to achieve better fertilization outcomes under postcopulatory competitive circumstances. Therefore, polyandry that intensifies post-mating sperm competition should constrain intraspecific sperm polymorphism. Contrary to this paradigm, we previously found that a polyandrous squid, Heterololigo bleekeri, produces dimorphic eusperm (flagellum length dimorphism; FLD), which is closely associated with alternative reproductive tactics (ARTs); large males (consorts) transfer their spermatophores inside the female’s mantle cavity, while small males (sneakers) do so outside the mantle. Thus, FLD was considered as the consequence of different insemination strategies that arise from different modes of sperm competition, sperm storage and the fertilization environment. However, in other squid species showing ARTs, the choice of mating behaviour is rather conditional (i.e., switching mating tactic between consorts and sneakers), which poses the question of whether sperm FLD could have evolved. Here, we investigated five species in the family Loliginidae that exhibit ARTs and found that all species showed sneaker-biased FLD. However, in a species with conditional ARTs, we found FLD rather ambiguous and the testicular somatic index to be nearly continuous among individuals at transitional state, suggesting that plasticity in mating behaviour compromises the disruptive selection on a sperm morphological trait.

Males conditionally inseminate at three female body locations according to female mating history and female maturity status in a squid

“…However, some loliginid squid species also show context-dependent ARTs 22 , 37 – 40 , where males flexibly change mating tactics in response to relative size differences between mating pairs 22 , 39 , which resulted in attenuated sperm dimorphism 40 . In any case, males must choose the designated areas of female body locations, because the insemination site greatly influences the fertilization success (but see 41 – 44 ).…”

“…Thus, in squid, the morphological traits of sperm are generally considered to be adaptive to the insemination environments and their associated sperm storage modes 36 . However, some loliginid squid species also show context-dependent ARTs 22,[37][38][39][40] , where males flexibly change mating tactics in response to relative size differences between mating pairs 22,39 , which resulted in attenuated sperm dimorphism 40 . In any case, males must choose the designated areas of female body locations, because the insemination site greatly influences the fertilization success (but see [41][42][43][44] ).…”

Squid male alternative reproductive tactics are determined by birth date

“…Furthermore, if they initially mature as a sneaker and switch to a consort tactic as they grow up, immature males larger than sneakers would not be observed during the reproductive season. Hirohashi et al [ 27 ] presumed the ARTs of H. bleekeri to be fixed because their reproductive traits are clearly dimorphic and no intermediate males were identified, unlike in D. plei [ 21 , 23 ]. Our result, indicating that most immature males had probably already determined their life-history pathway as a result of their hatch date, provides more direct support for this hypothesis.…”

“…In the present study, we also observed the growth history of H. bleekeri , but the environmental factors involved still remain to be determined, as do the ways in which they exert their influence based on hatch date to affect ART determination in H. bleekeri . In this species, distinct dimorphisms in reproductive traits, such as the form of spermatangia and sperm morphology, have been observed [ 25 – 27 , 51 ], and differences in gene expression have also been identified between the spermatozoa of consorts and sneakers [ 52 ]. Further epigenetic and endocrine studies to understand how the difference in hatch date influences the regulatory cascades underlying the phenotypic variation will help to further elucidate the mechanism of ART determination.…”

“…The Japanese spear squid Heterololigo bleekeri (Keferstein, 1866) is an ideal species to evaluate the birth date effect on ART determination in loliginid squid, since it is one of the most frequently studied cephalopods for research into ARTs [17,[24][25][26]. In this species, ARTs are considered to be fixed, unlike those of D. plei [27]. Furthermore, since H. bleekeri is widely distributed, extending to the highest latitude of any loliginid squid [28], it has a well-defined but long reproductive season (from January to May) and experiences seasonal changes in the environment [29], resulting in marked differences in growth conditions in its early life history between early-and late-hatched individuals.…”