The behavioural and molecular ecologies of the southern blue-ringed octopus, Hapalochlaena maculosa (Cephalopoda: octopodidae)

Morse, Peter (2017) The behavioural and molecular ecologies of the southern blue-ringed octopus, Hapalochlaena maculosa (Cephalopoda: octopodidae). PhD thesis, James Cook University.

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The cephalopods (Mollusca: Cephalopoda) provide a unique animal group for studying the mechanisms and genetic consequences of sexual selection. This is because: i) both males and females can be selective of their mates; ii) males can employ complex phenotypic-conditional mating strategies to secure copulations; iii) promiscuity of both sexes is widespread across this taxon despite no paternal care or resource provisioning by males for the females they mate with; and iv) females store sperm from multiple males until egg-laying, suggesting that sperm competition and cryptic female choice might be strong determinants of resulting fertilisation patterns. Additionally, nearly all cephalopods are relatively short-lived and invest heavily into their reproductive cycles. These characteristics suggest that sexually selected traits and behaviours can evolve rapidly within some cephalopods, making these taxa useful models for the examination animal mating system evolution and exploring mechanisms of speciation based on assortative mating, and pre- or postzygotic reproductive isolation.

The southern blue-ringed octopus (Hapalochlaena maculosa) is an endemic Australian octopod that displays several distinctive life-history traits making it an ideal study species for addressing hypotheses related to sexual selection and population divergence. This species has a seven-month life cycle, ending in a synchronous semelparous breeding season. Gametes are limiting for H. maculosa, with males and females possessing approximately 50 spermatophores or eggs per individual respectively. The females hold their small egg-clutches in their arms to protect and clean them until the time of hatching. The young are direct-developing, and so there is no planktonic dispersal phase. Together, these aspects of life history in H. maculosa suggest both that ensuring offspring quality might be particularly important for this species, and that short generation times with no larval dispersal might lead to rapid divergence of heritable traits and behaviours among geographically distant populations.

The present study addressed the mating behaviour and genetic structuring of H. maculosa by combining investigations of four separate components of behavioural and molecular ecology in this species. Precopulatory mate choice behaviours were investigated through focal animal observations in the laboratory. Postcopulatory fertilisation processes were assessed through paternity analyses using genotyped candidate parents. The roles of olfaction and social recognition were investigated by measuring the response of H. maculosa to conspecifics odours and comparing these responses to subsequent mate choice behaviours. Additionally, the broad-scale genetic structuring of H. maculosa was examined by obtaining 248 samples from across its geographic range, and using 17,523 single-nucleotide polymorphisms to identify patterns of population diversity, connectivity and local adaptation.

Focal animal observations showed no indication that females preferred to mate with males that displayed specific morphology or behaviour. However, females that terminated copulations mated longer with larger males. There was no indication of male preference for any female phenotypic traits, but male behaviours were consistent with theories of sperm competition, in that they spent more time in copulation with novel females, and females that had recently mated with higher numbers of competing males. Males mounted other males as frequently as they mounted females. However, male-male mounts were shorter than male-female mounts, suggesting that they might not be able to discriminate the sex of conspecifics until after they attempted to copulate.

Paternity analyses revealed multiple paternity in all genotyped egg-clutches. There was no relationship between either copulation time or mating chronology and the relative paternity of the candidate fathers, suggesting that differences in copulation durations observed in the first study might be related to mate guarding rather than sperm-loading or removal. Paternity of embryos along egg strings suggested that sperm might get mixed in the female oviducal gland, and paternal shares corresponded to remaining sperm signatures in maternal oviducal glands, post-egg deposition, in nine of twelve egg-clutches. Together these findings indicated it is unlikely for female H. maculosa to have the mechanical capacity to cryptically favour fertilisation by particular sperm she is holding. However, in one of the three cases where paternity did not correlate to residual sperm precedence, post-hoc analysis revealed that the male siring less paternity than expected was the female's full-sibling brother. This result anecdotally suggested that chemical processes might favour fertilisation to genetically compatible gametes post-copulation.

During odour cue trials, both male and female H. maculosa were observed to detect conspecifics via chemical cues in the water. Females responded to chemical signals differently based on the sex of the detected conspecific, but consistent with the prevalence of male-male mounts in the first study, males showed no evidence of sex discrimination using chemical cues. Females that reacted strongly to a male's odour were more likely to be unreceptive his copulation attempts one week later, and females spent less time in copulation with these males compared to males whose odour elicited a weaker response. This study concluded that response to conspecific odours might be related to agonistic behaviour and that females might react strongly to the odours of males they do not want to copulate with.

Broad-scale genetic analyses revealed that H. maculosa forms a clinal species pattern across its geographic distribution, from the southwest Australian coastline to Tasmania. The genetic divergence between H. maculosa sampled from distal ends of its range was consistent with the genetic differentiation observed between H. maculosa and its sister-taxon H. fasciata. However, the taxonomic identity of H. maculosa was maintained through small amounts of gene flow between adjacent populations across the entire species distribution. The genetic structuring of sampled populations was highly affected by both limited gene flow, due to its quick holobenthic life history, and strong patterns of local adaptation. This indicated that H. maculosa populations diverge rapidly and would be particularly susceptible to speciation if any barriers to dispersal and gene flow were to arise across its current species range. Diversity indices within populations indicated that individuals occupying the same habitat are highly related. Despite this pattern, indices also suggested that inbreeding might be rare in this species, strengthening findings in the third study that postcopulatory fertilisation patterns in H. maculosa might favour offspring to unrelated parents.

Collectively, studies carried out as part of this PhD, and included in this dissertation demonstrated that the unique life history of H. maculosa leads to a unique behavioural ecology. Limited gamete production and intense sperm competition have driven the development of dynamic male mating behaviours to ensure chances of fertilisation. Additionally, the lack of a dispersal phase resulting in high levels of interrelatedness within populations appear to have led to the large investment that H. maculosa puts towards promiscuity, and possibly postzygotic isolation, in order to ensure offspring sired to compatible partners. Further studies are required for verification of this hypothesis, however similar examples of ensuring genetic compatibility might help to explain the widespread occurrence of polyandry among the Cephalopoda.

Item ID: 52679
Item Type: Thesis (PhD)
Keywords: adaptive radiation, cryptic female choice, cryptic subspecies, ecological genomics, inbreeding avoidance, mate choice, octopus, operational sex ratio, paternity, polyandry, population genetics, SNP, sperm competition
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 3: Morse, Peter, Zenger, Kyall R., McCormick, Mark I., Meekan, Mark G., and Huffard, Christine L. (2015) Nocturnal mating behaviour and dynamic male investment of copulatory time in the Southern Blue-Ringed Octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae). Behaviour, 152. pp. 1883-1910.

Chapter 5: Morse, Peter, Zenger, Kyall R., McCormick, Mark I., Meekan, Mark G., and Huffard, Christine L. (2017) Chemical cues correlate with agonistic behaviour and female mate choice behaviour in the southern blue-ringed Octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae). Journal of Molluscan Studies, 83 (1). pp. 79-87.

Date Deposited: 10 Apr 2018 04:32
FoR Codes: 06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060308 Life Histories @ 30%
06 BIOLOGICAL SCIENCES > 0608 Zoology > 060801 Animal Behaviour @ 35%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 35%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 100%
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