Thorson's rule, life‐history evolution, and diversification of benthic octopuses (Cephalopoda: Octopodoidea)

Abstract

Here, we evaluate the so-called Thorson's rule, which posits that direct-development and larger eggs are favored toward the poles in marine organisms and whose validity been the subject of considerable debate in the literature, combining an expanded phenotypic dataset encompassing 60 species of benthic octopuses with a new molecular phylogeny. Phylogenetic reconstruction shows two clades: clade 1 including species of the families Eledonidae, Megaleledonidae, Bathypolypodidae, and Enteroctopodidae, and clade 2 including species of Octopodidae. Egg size, development mode, and all environmental variables exhibited phylogenetic signal, partly due to differences between the two clades: whereas most species in clade 1 inhabit cold and deep waters, exhibit large eggs and hatchling with holobenthic development, species from clade 2 inhabit tropical-temperate and shallow waters, evolved small eggs, and generally exhibit merobenthic development. Phylogenetic regressions show that egg size exhibits a conspicuous latitudinal cline, and that both egg size and development mode vary with water temperature. Additionally, analyses suggest that egg size is constrained by body size in lineages with holobenthic development. Taken together, results suggest that the variation in egg size and development mode across benthic octopuses is adaptive and associated with water temperature, supporting Thorson's rule in these organisms.

Testing adaptive hypotheses on the evolution of larval life history in acorn and stalked barnacles

“…Such a significant phylogenetic signal can be caused by developmental or genetic constraints, a low rate of evolutionary change, strong stabilizing selection, epistatic interactions with other traits, or adaptive radiation into similar niches (Harvey & Purvis, ; Losos, ; Revell, Harmon, & Collar, ; Wiens & Graham, ). Egg size, larval size, and larval developmental mode show signs of adaptive evolution because these traits, correlated with temperature, water depth, or chlorophyll a concentration (see e.g., Ibáñez et al, for similar conclusions). The combination of both strong phylogenetic and adaptive signals could be the result of phylogenetic niche conservatism, possibly caused by adaptive radiations of closely related species into similar niches (Ackerly, ; Harvey & Purvis, ).…”

“…Thorson's rule has been tested extensively using community or comparative datasets, and explains the geographic distribution of larval developmental mode in gastropods, bivalves, chitons, octopuses, anomurans, brachyurans, peracarids, holothuroids, and ophiuroids (e.g., Collin, ; Fernández, Astorga, Navarrete, Valdovinos, & Marquet, ; Pappalardo & Fernández, ; Ibáñez et al, ; see table 1 in Ibáñez et al, for a detailed compilation of studies analyzing Thorson's rule). Interestingly, several other studies, sometimes on the same taxa, did not find support for Thorson's rule (e.g., Pearse, for holothuroids and ophiuroids, Voight, for octopuses and Stanwell‐Smith, Peck, Clarke, Murray, & Todd, for Antarctic invertebrates).…”

“…Interestingly, several other studies, sometimes on the same taxa, did not find support for Thorson's rule (e.g., Pearse, for holothuroids and ophiuroids, Voight, for octopuses and Stanwell‐Smith, Peck, Clarke, Murray, & Todd, for Antarctic invertebrates). Ibáñez et al () suggest that these contrasting findings are the result of different analytical approaches, and a general lack of phylogenetic statistics (but see Pappalardo et al, ).…”

Global Patterns of Species Richness in Coastal Cephalopods

“…The Antarctic is assumed to be another center of origin of some deep-water fauna, including some groups of octopuses (Collins and Rodhouse, 2006;Strugnell et al, 2008;Xavier et al, 2018). The high endemism of benthic octopuses in this continent was supported by the evolution toward a holobenthic development that has influenced in situ speciation (Ibáñez et al, 2018).The historical causes entail isolation of the Antarctic fauna by (i) separation of the Antarctic continent from South America and Australia; and (ii) subsequent formation of the Antarctic Circumpolar Current, as the Drake Passage and Tasman gateway opened up around 30 Mya ago (Livermore et al, 2005;Scher et al, 2015). Strugnell et al (2008) estimated that the lineage of Antarctic (and deep-sea) octopuses diverged around 33 Mya (and radiated at 15 Mya).…”

Systematics and Phylogenetic Relationships of New Zealand Benthic Octopuses (Cephalopoda: Octopodoidea)

“…Considering that nearly 200 species are currently incorporated within this categorization, most of the octopod phylogenies published to date have included only few species (<30) (Carlini et al, 2001;Guzik et al, 2005;Strugnell et al, 2005;Strugnell et al, 2014), with just a few studies considering more than fifty species (see Lindgren et al, 2012;Ibáñez et al, 2014Ibáñez et al, , 2018. Incorporating much more species into octopod phylogenies seems problematic, as most species are recognized only from type material that has been fixed in formaldehyde and consequently lacks color and characters seen only in living specimens, and for which DNA sequences are not available.…”