Abstract
The cephalopods (Mollusca: Cephalopoda) are an exceptional class among the invertebrates, characterised by the advanced development of their conditional learning abilities, long-term memories, capacity for rapid colour change and extremely adaptable hydrostatic skeletons. These traits enable cephalopods to occupy diverse marine ecological niches, become successful predators, employ sophisticated predator avoidance behaviours and have complex intraspecific interactions. Where studied, observations of cephalopod mating systems have revealed detailed insights to the life histories and behavioural ecologies of these animals. The reproductive biology of cephalopods is typified by high levels of both male and female promiscuity, alternative mating tactics, long-term sperm storage prior to spawning, and the capacity for intricate visual displays and/or use of a distinct sensory ecology. This review summarises the current understanding of cephalopod reproductive biology, and where investigated, how both pre-copulatory behaviours and post-copulatory fertilisation patterns can influence the processes of sexual selection. Overall, it is concluded that sperm competition and possibly cryptic female choice are likely to be critical determinants of which individuals' alleles get transferred to subsequent generations in cephalopod mating systems. Additionally, it is emphasised that the optimisation of offspring quality and/or fertilisation bias to genetically compatible males are necessary drivers for the proliferation of polyandry observed among cephalopods, and potential methods for testing these hypotheses are proposed within the conclusion of this review. Further gaps within the current knowledge of how sexual selection operates in this group are also highlighted, in the hopes of prompting new directions for research of the distinctive mating systems in this unique lineage.
Highlights
Sexual selection is the competition within one or both sexes of a species toward optimising individual reproductive success (Darwin, 1906; Bateson, 1983)
The male uses the ligula to place each spermatophore at one of the openings to the female’s paired oviducts (Wells and Wells, 1972). This process can happen while the male is mounting the female’s mantle (e.g., Eledone spp. in Orelli, 1962; and Hapalochlaena spp. in Tranter and Augustine, 1973; Overath and Boletzky, 1974; Figure 9A), by the male reaching over to the female with the hectocotylus from a distance (e.g., O. digueti in Voight, 1991; and algae octopus, Abdopus aculeatus in Huffard et al, 2008; Figure 9B), or in a beak to beak mating position with the female at times enveloping the male in her web
Like in loliginid squid and cuttlefish, the high levels of female promiscuity, sperm storage and mate guarding all suggest, that in addition to differential copulatory rates, sperm competition most likely plays an influential role in male reproductive success within shallow-water octopus mating systems
Summary
Sexual selection is the competition within one or both sexes of a species toward optimising individual reproductive success (Darwin, 1906; Bateson, 1983). Sexual selection will often drive males of a species to develop traits or behaviours that enable them to achieve copulations with a higher number of females, to mate with healthier more fecund females and to attain greater fertilisation success with the females they mate with (Parker, 1970; Kodric-Brown and Brown, 1987; Reinhold et al, 2002). While females of the southern bottletail squid (Sepiadarium austrinum) can gain nutritional and likely fecundity benefits through the consumption of spermatophores (Wegener et al, 2013), in most cases females receive no identifiable resources or parental care from the males they mate with This suggests that male quality and/or genomic compatibility might be important factors in female mate selection, as observed in other animals (Jennions and Petrie, 1997; Tregenza and Wedell, 2000; Kokko et al, 2003). Biases in coverage by this review reflect the skew of existing behavioural research toward more accessible, abundant, and day-active species instead of offshore, nocturnal, and rarer forms
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