Sexual Selection and the Evolution of Male Reproductive Traits in Benthic Octopuses

Abstract

Competition between same-sex organisms, or intra-sexual selection, can occur before and after mating, and include processes such as sperm competition and cryptic female choice. One of the consequences of intra-sexual selection is that male reproductive traits tend to evolve and diverge at high rates. In benthic octopuses, females often mate with more than one male in a single reproductive event, opening the venue for intra-sexual selection at multiple levels. For instance, males transfer spermatophores through hectocotylus, and can remove the spermatophores left by other males. Considering the limited evidence on post-copula competition in benthic octopuses, and the potential to affect the evolution of reproductive traits within octopodids, we put this hypothesis to a test employing a phylogenetic comparative approach. We combined data on hectocotylized arm length (HAL), ligula length (LL), spermatophore length (SL) with a Bayesian molecular phylogeny of 87 species, to analyze how reproductive traits have diverged across lineages and covary with body size (mantle length; ML). First, additionally to ML, we estimated the phylogenetic signal (λ) and mode of evolution (κ) in each reproductive trait. Second, we performed phylogenetic regressions to quantify the association among reproductive traits and their co-variation with ML. This analysis allowed us to estimate the phenotypic change along a branch into the phylogeny, and whether selection may have played a role in the evolution and diversification of specific clades. Estimations of λ were always high (>0.75), indicating concordance between the traits and the topology of the phylogenetic tree. Low values of κ (<1.0) suggested that evolution depends on branch lengths. All reproductive traits exhibiting a positive relation with ML (β > 0.5 in all cases). Overall, evolutionary rate models applied to the SL-ML regression suggested that octopuses of the family Megaleledonidae have evolved larger spermatophores than expected for their size. The regression HAL-ML indicated that HAL was more variable in Megaleledonidae than in the remaining clades, suggesting that the high divergence across species within this group might partially reflect intra-sexual selection. These results support the hypothesis that, at least in some lineages, sexual selection may account for the divergence in reproductive traits of male octopuses.

Macroevolutionary Trade-Offs and Trends in Life History Traits of Cephalopods Through a Comparative Phylogenetic Approach

“…In this comparative study, we evaluated the life history traits of cephalopods considering their phylogenetic relationships, as suggested by Felsenstein (1985). This approach has been scarcely used in comparative studies of cephalopods, and particularly, the assessment of phylogenetic signal has only been conducted in five publications (i.e., Ibáñez et al, 2018Ibáñez et al, , 2019Ibáñez et al, , 2021Anderson and Marian, 2020;Ponte et al, 2021). In this sense, our research is among the few studies correctly addressing trait comparisons for cephalopods, suggesting that further research should incorporate this approach in comparative biology of cephalopods.…”

“…In this context, natural selection could benefit some of these strategies under fluctuating environmental conditions, for example, increasing the fitness of squids by enabling the production of millions of eggs (e.g., A. dux, D. gigas) owing to the energetic costs and strong selective pressures (Ramirez-Llodra, 2002). In this context, evidence also suggests phenotypic selection on sexual traits in octopuses driven by sexual selection via sperm competition and cryptic female choice (Ibáñez et al, 2019). Hence, it is expected that the copulatory organs of squids, sepiolids and other cephalopods also exhibit phenotypic selection, suggesting that not only the environment can exert selective pressures on cephalopods, as on other marine ectotherms, but also the intraspecific interactions associated with biological fitness.…”

“…Over 30 years ago, Felsenstein (1985) suggested that every study addressing comparative biology should consider the phylogenetic relationships of the group being evaluated, as most biological features are associated with the evolutionary history of living organisms. For this reason, several studies have shown the importance of including phylogenetic relationships in comparative studies of either physiological (Rezende and Diniz-Filho, 2012), reproductive (Ibáñez et al, 2018(Ibáñez et al, , 2019(Ibáñez et al, , 2021, or biogeographic traits (Hernández et al, 2013). In this context, comparative studies not including phylogeny violate data independency assumptions, being susceptible to spurious associations between traits (type I errors) or to mask true associations (type II errors) (Felsenstein, 1985;Rezende and Diniz-Filho, 2012).…”

The shape of sucker ring teeth in the hectocotylized part of kisslip cuttlefish (Sepia lycidas)

“…Cephalopod mating behavior is very unique as it is carried out using a modified arm. Most male cephalopods have a modified arm called the hectocotylus, which is used for transferring a batch of spermatophores to females (Drew, 1911;Squires et al, 2013;Hanlon, Messenger, 2018;Ibáñez et al, 2019). The hectocotylus was first described in Aristotle's work.…”

A Theoretical Comparison of Alternative Male Mating Strategies in Cephalopods and Fishes

“…Interestingly, sneaker males also occur in phylogenetically completely unrelated cephalopods: cuttlefish, octopi and squid (Tsuchiya & Uzu, 1997; Norman et al, 1999; Hall & Hanlon, 2002; Ibáñez, 2019; Marian et al, 2019; Brown et al, 2021; Apostólico & Amoroso RodriguezMarian, 2020). In these species, just as in fishes, smaller males without a territory of their own clandestinely achieve matings with females, sometimes while taking up a female-like coloration (which is behaviorally plastic at fast time-scales in cephalopods).…”