Mating Behaviour and Postcopulatory Fertilization Patterns in the Southern Blue-Ringed Octopus, Hapalochlaena Maculosa

Animal Behaviour 136 (2018) 41e51

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Animal Behaviour

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Mating behaviour and postcopulatory fertilization patterns in the southern blue-ringed octopus, Hapalochlaena maculosa

* Peter Morse a, d, , Christine L. Huffard b, c, Mark G. Meekan a, Mark I. Mccormick d, Kyall R. Zenger d a Australian Institute of Marine Science, C/o UWA OI (MO96), Crawley WA, Australia b Monterey Bay Aquarium Research Institute, Moss Landing, CA, U.S.A. c California Academy of Sciences, San Francisco, CA, U.S.A. d College of Science and Engineering, James Cook University, Townsville, QLD, Australia article info Female octopuses are known to store sperm from multiple males they encounter throughout a breeding Article history: season, before laying a single clutch with mixed paternity. Although octopuses display a broad range of Received 23 March 2017 precopulatory behaviours, and both sperm competition and cryptic female choice have been hypothe- Initial acceptance 29 May 2017 sized to occur, the current understanding of how these processes influence resulting paternity remains Final acceptance 6 November 2017 limited. This study aimed to identify behavioural factors associated with paternity patterns and the capacity of females to bias paternity postcopulation to specific males in the southern blue-ringed MS. number: 17-00260R octopus, Hapalochlaena maculosa. Genetic markers and controlled, sequential, laboratory pairings of genotyped individuals were used to examine paternity patterns and compare them to relative signatures Keywords: of male sperm remaining in female oviducal glands after egg laying. Multiple paternity was discovered in cryptic female choice all 12 laboratory-reared clutches. There was no indication that the relative time spent in copulation inbreeding avoidance affected the resulting paternity. Males that waited for females to terminate the copulation had greater paternity fi polyandry paternity when they were the rst candidate male, but this was not the case among second candidate SNP males. The relative quantities of candidate male alleles detected in female oviducal glands after egg laying were consistent with relative paternity of the candidate males in all but three cases. In one of these, sibship analysis revealed that the male that obtained less paternity than expected was in fact the female's full-sibling brother. Although this study found no evidence for female postcopulatory selection of male sperm, anecdotal evidence suggests that female H. maculosa might benefit from polyandry if chemical processes can favour clutch fertilization by unrelated males. Future studies, investigating paternity bias among genotyped males of varying, but known relatedness to the female, might help to validate this pattern. © 2017 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Promiscuity, or extrapair copulation, is a common occurrence in males can provide the female with increased resources or paternal animal mating systems (Bateson, 1983). Promiscuity among males care (Jennions & Petrie, 1997; Reynolds & Gross, 1990). However, (polygyny), which often have abundant and low-cost sperm polyandry might be less common among species where females do (Kodric-Brown & Brown, 1987), can easily develop as an evolu- not receive material resources or parental care from the males they tionarily stable strategy (Maynard Smith, 1982). This is because mate with (Jennions & Petrie, 2000). This is because females have a copulating with additional females leads to more offspring, thereby finite number of eggs they can lay in a lifetime (Kodric-Brown & directly increasing male reproductive success (Bateson, 1983). Brown, 1987), and therefore the number of offspring they can Promiscuity among females (polyandry), which typically have more produce is not typically limited by the numbers of males they costly gametes (Kodric-Brown & Brown, 1987), can also easily copulate with (Bateson, 1983). Additionally, copulating with mul- evolve within mating systems where copulating with additional tiple males can potentially be costly to females because of the increased risk of potential harm during copulations (Adamo et al., 2000; Hoving, Lipinski, Videler, & Bolstad, 2010), decreased * Correspondence: P. Morse, Australian Institute of Marine Science, c/o UWA OI foraging time (Huffard, Caldwell, & Boneka, 2008), increased risk of (MO96), Crawley, WA, 6009, Australia. disease transfer (Thrall, Antonovics, & Dobson, 2000) and increased E-mail address: [email protected] (P. Morse). https://doi.org/10.1016/j.anbehav.2017.12.004 0003-3472/© 2017 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 42 P. Morse et al. / Animal Behaviour 136 (2018) 41e51 energy expenditure (Franklin, Squires, & Stuart-Fox, 2012). There- Hanlon, 2002; Huffard et al., 2008; Morse, 2008; Morse, Zenger, fore, it is generally presumed that where polyandry exists, and male McCormick, Meekan, & Huffard, 2015; Wada, Takegaki, Mori, & provision of resources or parental care does not, that promiscuous Natsukari, 2005a), suggest that the function(s) of polyandry in females might benefit from additional copulations indirectly, by cephalopod life histories are probably more complex and yet to be maximizing the genetic quality rather than quantity of their wholly understood. offspring (Jennions & Petrie, 2000; Simmons, 2005; Zeh & Zeh, Polyandrous behaviour may also be selected for in cephalopod 1996, 1997). When this is the case, a higher offspring quality can mating systems if postcopulatory fertilization processes can in- lead to increased success in the F2 generation (grandchildren), and crease the likelihood of promiscuous females siring viable and/or this can be the selective advantage necessary for polyandry to sexually prolific offspring (Kirkpatrick, 1982; Tregenza & Wedell, become an evolutionarily stable strategy within a species 2002; Yasui, 1997). Theoretically, if females can assess male geno- (Kirkpatrick, 1982; Maynard Smith, 1982). types and have control over which males' sperm they use to It can be difficult to quantify the indirect advantages that fe- fertilize their eggs, they could increase their fitness by mating with males might obtain from polyandrous mating systems (Slatyer, multiple males as they encounter them within a breeding cycle and Mautz, Backwell, & Jennions, 2012). However, the cephalopods then preferentially use sperm from the highest quality and/or most (Mollusca: Cephalopoda) are ideal for investigating this subject, genetically compatible male(s) postcopulation (Eberhard, 1996; because polyandry is widespread among this class (Hanlon & Tregenza & Wedell, 2002; Zeh & Zeh, 1997). This mechanism is Messenger, 1998). It has been observed in every cephalopod mat- referred to as ‘cryptic female choice’ and can occur if the female is ing system studied to date, despite limited evidence for male pro- able to use either physical or chemical processes to influence the vision of resources or paternal care (Hanlon & Messenger, 1998; but probability of a male's sperm successfully fertilizing her egg(s) see spermatophore consumption in the southern bottletail squid, (Eberhard, 1996). This could potentially happen in a variety of ways Sepiadarium austrinum:;Wegener, Stuart-Fox, Norman, & Wong, among the Cephalopoda and would depend on the species' 2013; and possible food-sharing behaviour in the larger Pacific morphology. For example, in sepiids (Sepioidae: Sepiidae) and most striped octopus, Octopus sp.: Caldwell, Ross, Rodaniche, & Huffard, teuthoids (Cephalopoda: Teuthoidea) which have external sper- 2015). Additionally, female cephalopods can store sperm from the matophore placement and fertilization (Mangold, 1987, pp. multiple males they mate with (Mangold, 1987, pp. 157e200), and 157e200; but cf. Hoving & Laptikhovsky, 2007), the females could the resulting fertilization of their eggs could potentially be influ- simply use their arms to select sperm left in their storage organs enced by a suite of complex interactions documented within their and mantle exteriors from preferred males at the time of fertil- mating systems (Hanlon & Messenger, 1998). Some of these mating ization (Naud et al., 2005, 2016). Previous studies have also sug- behaviours include phenotypic-conditional male mating strategies gested that some female cephalopods could influence fertilization (Hanlon, Smale, & Sauer, 2002; Huffard et al., 2008; Norman, Finn, patterns by ejecting sperm from their storage organs (Buresch et al., & Tregenza, 1999), multiple types of positioning during copulation 2009; Sato, Yoshida, & Kasugai, 2016), controlling the timing be- (Huffard & Godfrey-Smith, 2010; Iwata, Munehara, & Sakurai, tween copulations and egg laying (Buresch et al., 2009; Squires 2005; Jantzen & Havenhand, 2003) and differential placement of et al., 2015), and regulating copulation durations with males to sperm packages (Buresch, Maxwell, Cox, & Hanlon, 2009; Hanlon, control how much sperm is transferred to them in the first place Maxwell, & Shashar, 1997, 2002; Jantzen & Havenhand, 2003; (Morse, 2008). However, the current understanding of the context Naud, Shaw, Hanlon, & Havenhand, 2005). Where genetic for these behaviours and how they may affect paternity patterns is markers have been used, they have confirmed these behaviours still sparse (cf. Buresch et al., 2009; Squires et al., 2015; Naud et al., lead to multiple paternity (Buresch et al., 2009; Iwata et al., 2005; 2016; Sato et al., 2016). Morse, 2008; Naud, Hanlon, Hall, Shaw, & Havenhand, 2004; Octopuses (Octopoda: Octopodidae) and sepiolids (Sepioidae: Naud, Sauer, McKeown, Shaw, 2016; Shaw & Sauer, 2004; Squires, Sepiolidae), which have internal fertilization (Mangold, 1987, pp. Wong, Norman, & Stuart-Fox, 2014; Squires, Wong, Norman, 157e200), could theoretically use muscles to pump sperm selec- Stuart-Fox, 2015). However, the role that these behaviours play in tively from the oviducal glands, where sperm is stored, during defining paternity patterns and the resulting selection within these fertilization (Froesch & Marthy, 1975), or possibly time the release mating systems remains largely unknown (cf. Squires et al., 2015). of sperm-attractant peptides to preferentially store spermatozoa Finally, it has been found that extra copulations can be metaboli- and/or activate it during fertilization (De Lisa, Salzano, Moccia, cally demanding for at least one female cephalopod (dumpling Scaloni, & Di Cosmo, 2013). Despite cryptic female choice having squid, Euprymna tasmanica, Franklin et al., 2012), which empha- long been hypothesized to occur in octopuses, evidence to support sizes that female promiscuity must also yield a fitness benefitto this mechanism is currently lacking due to it being more difficult to compensate for this extra cost. assess biased sperm use within animals that have internal It has been suggested that polyandry may have evolved within fertilization. some cephalopod mating systems as a form of bet-hedging strat- Several male behaviours could also impact paternity patterns in egy, whereby females can ensure their fitness by mating with cephalopod mating systems (Cigliano, 1995; Hall & Hanlon, 2002; multiple males to obtain a more genetically diverse clutch Hanlon et al., 1997; Wada, Takegaki, Mori, & Natsukari, 2005b, (Quinteiro et al., 2011). It has also been pointed out that proteins in 2006). Mate-guarding behaviours have been observed across the seminal fluid can provide additional nutrition for females that many cephalopod taxa in both the laboratory (Adamo et al., 2000; engage in more copulations, and this might provide promiscuous Wada et al., 2006) and field (Hall & Hanlon, 2002; Hanlon et al., females with a direct fitness benefit(Fedorka & Mousseau, 2002; 2002; Huffard et al., 2008; Jantzen & Havenhand, 2003). Sperm- Squires, Wong, Norman, & Stuart-Fox, 2012). While the above loading behaviours have also been suggested to help males in- two mechanisms can certainly explain selective advantages to crease their chances of successful fertilization with females in the polyandrous females, observations of complex and often biased presence of competing males' sperm (Hall & Hanlon, 2002; Hanlon paternity patterns (Shaw & Sauer, 2004; Iwata et al., 2005; Naud et al., 1997; Huffard et al., 2008; Jantzen & Havenhand, 2003; Wada et al., 2005, 2016; Morse, 2008; Buresch et al., 2009; but see ; et al., 2006). Additionally, male sperm removal has been observed Squires et al., 2014), as well as widespread observations that female in several sepiids (Hall & Hanlon, 2002; Hanlon, Ament, & Gabr, cephalopods often reject male copulation attempts (Adamo et al., 1999; Wada et al., 2005b, 2006, 2010), and has been proposed to 2000; Cheng & Caldwell, 2000; Corner & Moore, 1981; Hall & occur in some octopuses based on mating behaviour (Cigliano, Download English Version: https://daneshyari.com/en/article/8488668

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