Evidence of sperm removal behaviour in an externally fertilizing species and compensatory behaviour for the risk of self-sperm removal

Abstract

The removal of rival sperm from a female's sperm storage organ acts as a strong sperm competition avoidance mechanism, which has been reported only in internally fertilizing species and not at all in externally fertilizing species. This study demonstrated for the first time that nest-holding males of Bathygobius fuscus , an externally fertilizing marine fish, remove the sperm of rival sneaker males from the spawning nest by exhibiting tail-fanning behaviour within the nest. Males showed tail-fanning behaviour when semen was artificially injected into the nest but not when seawater was injected, and in open nests this behaviour resulted in higher paternity rates for the focal male. The sperm removal behaviour entails the risk of removing their own sperm; therefore, additional sperm release behaviour is likely necessary to benefit from the sperm removal effect. Consistent with this, males increased post-fanning sperm release behaviour more in the semen than in the seawater injection treatment. Moreover, males who had removed sperm for a longer time spent more time releasing sperm after the removal, suggesting that the additional sperm release behaviour compensated for the loss of their own sperm. These results suggest that sperm removal behaviour is not restricted to internally fertilizing organisms and deserves further investigation in this and other species.

Sperm adaptation in relation to salinity in three goby species

“…In a closed nest cavity, a single long‐lived sperm ejaculation could remain in the nest and fertilize eggs from several females. Recently, in the dusky frillgoby with similar nesting behaviour as the sand goby, nest guarding males were shown to use tail fanning to remove sperm from other males (Takegaki et al ., 2020). Furthermore, in many gobies males prepare the spawning surface with a sperm containing mucus trail from which new sperm are activated over time, as the mucus dissolves (Marconato et al ., 1996; Scaggiante et al ., 1999; Svensson & Kvarnemo, 2005), creating a further reason for increased longevity of sperm.…”

Molecular, behavioural and morphological comparisons of sperm adaptations in a fish with alternative reproductive tactics

“…Compared with many other fishes, whose sperm stay motile for seconds or minutes (Browne et al, 2015 ), this is remarkable. It is hard to speculate what selective pressures and steps have allowed such long‐lived sperm to evolve; however, it means that once ejaculated, sperm may retain their fertilisation ability for a very long time as long as they are not swept away by currents or (in the case of sneaker male sperm) removed by vigorous fanning by the nest‐holder (Takegaki et al, 2020 ). Further, extended sperm longevity is likely to offer a similar function to the sperm‐containing mucus (Marconato et al, 1996 ), that is, releasing the male from the need to stay close to the spawning female, freeing him to defend the nest from intruders.…”

“…However, sneaker males may also have long‐lived sperm. Accordingly, in Bathygobius fuscus , nest‐holding males have been shown to remove sneaker male sperm from the nest by vigorously fanning the tail (Takegaki et al, 2020 ).…”

How sexual and natural selection interact and shape the evolution of nests and nesting behaviour in fishes

“…In sand gobies, males build sand burrows with small nest openings in the presence of sneaker males ( box 2 ) [ 52 ] and in the Lake Tanganyika cichlid Lamprologus lemairii, paternity correlates negatively with nest-site opening width [ 155 ]. However, in species that remove rival male sperm by fanning [ 156 ], a small nest opening may make sperm removal less effective. In L. callipterus (§§2a and 4e), a genetically determined dwarf male strategy has evolved as an adaptation to both the shells and the large territorial males.…”