Rare polyandry and common monogamy in the firefly squid, Watasenia scintillans

Abstract

In cephalopods, all species are considered to be polyandrous because of their common life history and reproductive traits reflecting a polyandrous mating system. Contrary to this belief, here we show several lines of evidence for monogamy in the firefly squid, Watasenia scintillans. In this species, females are capable of long-term storage of spermatangia, and of egg spawning even after the complete disappearance of males following the breeding season. The stored spermatangia are distributed equally between bilateral pouches under the female's neck collar. Such a nonrandom pattern of sperm storage prompted us to hypothesize that females might engage in lifetime monandry. Hence, we genotyped female-stored spermatangia and offspring, and found that in 95% of females (18/19), all the spermatangia had been delivered from a single male and all the embryos in a clutch had been sired by spermatozoa from stored spermatangia. In males, throughout the reproductive season, relative testis mass was much smaller in W. scintillans than in all other cephalopods examined previously. The mean number of male-stored spermatophores was ~ 30, equivalent to only 2.5 matings. Our genetic, demographic and morphometrical data agree with a mathematical model predicting that monogyny is favored when potential mates are scarce. Together, these results suggest mutual monogamy in W. scintillans.

Figure 1

The mode of and change in sperm storage throughout the reproductive season in W. scintillans. (A) Population dynamics of males and mated females from January to May. A cyan box indicates the estimated mating period. Total of 1,414 males and 4,733 females were analyzed. (B) A dorsal view of the female around the neck. Arrowheads point to the spermatangia visible through the transparent mantle. (C) A single mass of spermatangium with unidirectionally oriented ejaculatory ducts (arrowheads). (D) Spermatozoa stored in the spermatangia. (E) An anatomical illustration of the female seminal receptacle along the body axis (A, anterior; P, posterior). (F) A heatmap represents the frequency of female individuals having different patterns of spermatangium number on bilateral sides of the seminal receptacle. Histograms show frequency distribution of spermatangium number for each side (upper left and upper right) and left–right symmetry (bottom). (G) No seasonal change in number of spermatangia stored in females. Total of 1,400 females were examined.

Figure 2

Paternity analysis of each spermatangium stored on the females. Using a total of nineteen females, every single spermatangium was isolated and genotyped. Each column represents paternity share by the first (filled box), second (diagonal stripes) and third (jagged stripes) male. Open box indicates unidentified paternity.

Figure 3

Allocation of male reproductive resources in W. scintillans and other squids. (A–E) In W. scintillans, seasonal changes in the number of male-storing spermatophore (A), mantle length (B), body weight (C), testicularsomatic indices (D) and ovariansomatic indices (E) are plotted as the mean ± SE. Data points represent males in blue and females in red. Cyan boxes indicate the estimated mating period. For (A–E), total of 402 males and 950 females were examined. (F) A graph showing a comparison of male testicularsomatic indices among previously reported cephalopod species and W. scintillans found in this study (*). Data were extracted from the literature indicated by reference # (Table S1). The columns indicate the mean (blue column) or minimum (gray column) values specified in the literature, otherwise mean values were estimated (gradient column) from presented data points in the graphs. (G, H) The GSI values from male individuals are plotted against number of spermatophore (G, H) or testis weight (I, J) in W. scintillans (G, I) and highly promiscuous Idiosepius paradoxus (H, J). (K, L) In each individual, allocation of male reproductive resources to testis (K) or spermatophore (L) is expressed in percentage.