Molecular Phylogenetics and Evolution 120 (2018) 212–217

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Molecular Phylogenetics and Evolution

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Short Communication Updated molecular phylogeny of the squid family Ommastrephidae: Insights T into the evolution of spawning strategies ⁎ M. Cecilia Pardo-Gandarillasa, Felipe I. Torresa,b, Dirk Fuchsc, Christian M. Ibáñezb, a Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Las Palmeras 3425, Ñuñoa, Santiago, Chile b Departamento de Ecología y Biodiversidad, Facultad de Ecología y Recursos Naturales, Universidad Andres Bello, República 440, Santiago, Chile c Department of Natural History Sciences, Hokkaido University, Sapporo, Hokkaido, Japan

ARTICLE INFO ABSTRACT

Keywords: Two types of spawning strategy have been described for ommastrephid squids: coastal and oceanic. It has been Cephalopoda suggested that ancestral ommastrephids inhabited coastal waters and expanded their distribution into the open Evolution ocean during global changes in ocean circulation in the Oligocene. This hypothesis could explain the different Reproduction reproductive strategies in oceanic squids, but has never been tested in a phylogenetic context. In the present Ancestral states study, we assess the coastal-to-open-ocean hypothesis through inferring the evolution of reproductive traits Divergence times (spawning type) of ommastrephid squids using the phylogenetic comparative method to estimate ancestral states and divergence times. This analysis was performed using a robust molecular phylogeny with three mitochondrial genes (COI, CYTB and 16S) and two nuclear genes (RHO and 18S) for nearly all species of ommastrephid squid. Our results support dividing the Ommastrephidae into the three traditional subfamilies, plus the monotypic subfamily Todaropsinae as proposed previously. Divergence times were found to be older than those suggested. Our analyses strongly suggest that early ommastrephid squids spawned in coastal areas, with some species subsequently switching to spawn in oceanic areas, supporting previous non-tested hypotheses. We found evi- dence of gradual evolution change of spawning type in ommastrephid squids estimated to have occurred since the Cretaceous.

1. Introduction species would be characterized by long periods of stasis followed by short punctuated bursts of evolution associated with speciation Environmental changes in geological and ecological dimensions (Eldridge and Gould, 1972; Pagel et al., 2006). Phylogenetic evidence have been proposed to promote the evolution of species across a broad attributes great importance to punctuated models of evolution in pro- spectrum of biological aspects (e.g., life histories, distribution, specia- moting rapid evolutionary divergence in different organisms (Pagel lization, speciation, extinction) (Dynesius and Jansson, 2000; Schoener, et al., 2006). To assess the effects of gradual evolution on certain traits, 2011). In the marine environment, the evolution of life forms from some sophisticated phylogenetic approaches have been developed to benthic to nektonic reflects a progressive evolution related to sea level scale the relationship between individual phylogenetic branch lengths changes in different modern taxonomic groups (e.g., fishes, cephalo- and trait evolution (e.g., Pagel et al., 2006). pods, reptiles and mammals; Nesis, 1978). In modern cephalopods, Squids of the family Ommastrephidae are the most abundant, Lindgren et al. (2012) reported convergent evolution of multiple phe- widely distributed, ecologically active cephalopods (Wormuth, 1998). notypic traits correlated with habitat type. Nigmatullin (1979, 2007) Traditionally the family has been divided into three subfamilies (Om- proposed the hypothesis that oceanic and coastal spawning in om- mastrephinae, Todarodinae and Illicinae) based on morphological mastrephid squids evolved in relation to environmental changes during traits, such as the structures of the funnel groove, morphology of the the Oligocene – Miocene transition and the radiation of scombrid fishes. club suckers and hectocotylus, and presence and placement of photo- These evolutionary patterns suggest the influence of gradual change as phores (Roeleveld, 1988; Wormuth, 1998). Although due to peculia- predicted by phyletic gradualism theory, but in some cases the observed rities in morphological traits it has been proposed creating two addi- rate of evolution is faster than expected according to this theory tional subfamilies Ornithoteuthinae (Nigmatullin, 1979) and (Eldridge and Gould, 1972). Rapid evolution is related to punctuated Todaropsinae (Nigmatullin, 2000) to place Ornithoteuthis and Todaropsis equilibrium, a theory that suggests evolutionary divergence among respectively, the three-subfamily classification prevails (Wormuth,

⁎ Corresponding author. E-mail addresses: [email protected], [email protected] (C.M. Ibáñez). https://doi.org/10.1016/j.ympev.2017.12.014 Received 16 February 2017; Received in revised form 3 November 2017; Accepted 11 December 2017 Available online 14 December 2017 1055-7903/ © 2017 Elsevier Inc. All rights reserved. M.C. Pardo-Gandarillas et al. Molecular Phylogenetics and Evolution 120 (2018) 212–217

1998; Wakabayashi et al., 2012). According to their spawning location, the substitution model GTR+G+I. The clock rate was estimated using ommastrephid squids can be classified into coastal and oceanic. Coastal a relaxed clock with an uncorrelated lognormal distribution. The Birth- spawning (on the continental shelf) is common among the subfamilies Death model served as the tree prior, and parameters were logged every Illicinae and Todarodinae, it is characterized by a long maturation 1000 iterations, to a sample total of 20,000,000 generations. Burn-in period without somatic growth, and intermittent spawning with de- was determined by Tracer, accounted for the initial 10% of the first creasing intensity (with potential fecundity of 0.04–2.5 million, estimation, and was discarded from calculations. The best evolution Nigmatullin and Laptikhovsky, 1994; Nigmatullin, 2007). Notable ex- model of the molecular clock (strict or relaxed) was evaluated by ceptions however include the two species of Ornithoteuthis (according to comparing Bayes Factors, adjusting the molecular clock using four ca- Wakabayashi et al., 2012 a member of the Todarodinae), these are libration points. The first one was the split between Decapodiformes known to spawn far from the shore, as O. antillarum which has been and Octopodiformes (Carninan, 236 Mya; Kröger et al., 2011) with a recorded spawning around seamounts (Nigmatullin and Laptikhovsky, gamma distribution and the following parameters: offset = 236, 1994). Oceanic spawning is characteristic of Ommastrephinae, which shape = 2.0, scale = 3.0. The second calibration point was the diver- display quick maturation with somatic growth and multiple spawning gence of Vampyromorpha and Octopodiformes using genus Teudopsis over several months with relatively stable intensity (potential fecundity from the Lower Jurassic (Toarcian, 182 Mya; Fuchs and Weis, 2008), 0.1–32 million, Nigmatullin and Laptikhovsky, 1994; Nigmatullin, The third calibration point used was the origin of Myopsida using lo- 2007). Nigmatullin (1979, 2007) suggesting that ancestral ommas- liginid statoliths from the mid-Eocene (48 Mya; Neige et al., 2016) with trephids used to inhabit coastal waters and then expanded their ranges gamma distribution and the following parameters: offset = 48, to open ocean during the Oligocene due to global ocean circulation shape = 2.0, scale = 1.0, and the final one was the split of northern and changes. This historical change of habitat could explain the origin of southern Atlantic (USA vs Brazil) genetic lineages of Doryteuthis pleii: different spawning strategies for oceanic and coastal squids offset = 16 Mya (Sales et al., 2017), shape = 2.0, scale = 1.0. (Nigmatullin, 2007), implicating that there may have been a gradual The evolution of the reproductive type (oceanic and coastal evolution of reproductive strategies on a par with slow changes in ha- spawning) was evaluated using the multistate model on BayesTraits v.3 bitat. Although insightful, the ideas proposed by Nigmatullin (1979, (http://www.evolution.rdg.ac.uk/BayesTraitsV3/BayesTraitsV3.html). 2007) were never statistically tested. The evolution of a binary trait (0 = coastal and 1 = oceanic) was The main purpose of the present study is to test previous ideas on modelled estimating two parameters, a rate of change from 0 to 1 (q01) the evolution of ommastrephid spawning by using quantitative tech- and a rate of change from 1 to 0 (q10), assuming these two rates are niques for the first time. We apply the phylogenetic comparative equal. In order to estimate these rate of change, we used the informa- method which is based on a robust Bayesian molecular phylogeny with tion about the distribution of 0 s and 1 s at the tips of the trees (i.e. for mitochondrial and nuclear genes for 18 out of the 22 extant ommas- each species), and the branch lengths of these trees. Through a Bayesian trephid species. framework the rate of gain (q01) and loss (q10) of the spawning type was estimated in each branch of the 1000 phylogenetic random trees 2. Materials and methods selected from a sample of trees, using BayesTrees v.1.3 (http://www. evolution.reading.ac.uk/BayesTrees.html). A beta hyperprior was used Through a literature review we acquired information on re- for q10 and q01 (α =2,β = 2). Additionally, the most recent common productive strategy from 18 ommastrephid species (see supplementary ancestor together with posterior probability of ancestral reproductive material). For phylogenetic reconstruction analyses, sequences were strategy (P(0) = coastal spawning, P(1) = oceanic spawning) was cal- obtained from Genbank (supplementary material, Table S1) for three culated for the basal nodes of the trees. For this analysis of character mitochondrial and two nuclear genes: 16S rRNA (16S), Cytochrome evolution, 20,000,000 iterations of MCMC were ran, sampling para- Oxidase I (COI) and Cytochrome b (CYTB); and Rhodopsin (RHO) and meters every 1000 iterations, discarding the first 10% of parameters as 18S rRNA (18S), respectively. burn-in. In addition, the Kappa parameter (κ) was estimated to infer The best nucleotide substitution model was estimated by Bayesian whether evolution of spawning type is related with a gradual (κ =1)or Information Criterion (BIC) implemented in jModelTest (http:// punctuated (κ < 1) model of evolution. An analysis was performed to evomics.org/learning/phylogenetics/jmodeltest/) for each gene. The test gradual evolution on traits, setting the kappa parameter to κ =1 phylogenetic reconstruction was inferred from a partition matrix da- and comparing it with κ as estimated by Bayes Factor. Outgroups were taset with different substitution models for each gene, and another excluded from the analyses performed using “Exclude Taxa” command matrix including the concatenated dataset (16S+COI+CYTB+RHO in BayesTraits. +18S) using the most complex model (GTR+G+I). Both analyses were compared by means of Bayes Factors (BF) in Tracer v.1.5 (http://tree. 3. Results bio.ed.ac.uk/software/tracer/). To evaluate the evolutionary relation- ships, a phylogenetic hypothesis based on a Bayesian framework We found GTR+G+I to be the best model to obtain high posterior (MrBayes v.3.2, http://mrbayes.sourceforge.net/) was used to obtain a probabilities in the phylogeny (−ln = 9558.08, BF = 6.89) using a sample of trees, which allowed the inclusion of phylogenetic un- concatenated matrix (16S+COI+CYTB+RHO+18S). The phyloge- certainty in subsequent analyses using the comparative method. Four netic reconstruction showed three major clades corresponding to the chains were run with 10,000,000 iterations by means of Metropolis three subfamilies (Illicinae, Ommastrephinae, Todarodinae; Fig. 1). Coupled Markov Chains Monte Carlo (MCMCMC), sampling parameters Excluding COI we found the same topology (Fig. S1). and trees every 1000 iterations. Trees were rooted using Vampyropoda To estimate the divergence time, the model that best fitted the data (Vampyromorpha + Incirrata) and 23 species belonging to families was the relaxed and uncorrelated molecular clock with lognormal dis- Spirulidae, Sepiidae, Loliginidae, Onychoteuthidae, Gonatidae and tribution (−ln = 33491.41, BF > 0.5). In this context, the mean of Architeuthidae which combined, have been described as a sister group divergence time estimation for Ommastrephidae (Clade 1) occurred of ommastrephids (Lindgren et al., 2012). Additionally we performed a 87.1 Mya (High Posterior Density, HPD, 95%, 65.9–108.7 Mya, Fig. 2) phylogenetic analysis excluding COI to evaluate whether this gene during the Upper Cretaceous; for Ommastrephinae (Clade 2) 60.9 Mya distorts the evolutionary relationships among cephalopods (Supple- (41.7–80.7 Mya HPD 95%) during the Paleocene and divergence of the mentary material, Fig. S1). Todarodinae and Illicinae + Todaropsis eblanae (Clade 3) would have A Bayesian MCMC divergence times analysis was performed using occurred during the Upper Cretaceous (78.9 Mya 60.4–90.1 Mya HPD BEAST v.1.8.4 (http://beast.community/) for the molecular clock, 95%, Fig. 2). For Illicinae + Todaropsis eblanae (Clade 4) 70.1 Mya HPD using the concatenated data set (16S+COI+CYTB+RHO+18S) and 46.1–95.1 and subfamily Illicinae (Clade 5) 16.5 Mya (8.3–28.7 Mya

213 M.C. Pardo-Gandarillas et al. Molecular Phylogenetics and Evolution 120 (2018) 212–217

Outgroups

0.92 Todaropsis eblanae

Illex argentinus

Node 2 1.0 Illex illecebrosus 1.0 Illex coindetii

1.0 1.0 Hyaloteuthis pelagica Eucleoteuthis luminosa

Ommastrephes bartramii Node 1 Node 3 0.87 Dosidicus gigas 0.79 Sthenoteuthis oualaniensis 1.0 0.97 Sthenoteuthis pteropus Ornithoteuthis volatilis 1.0 Ornithoteuthis antillarum 1.0 1.0 Todarodes filippovae 1.0 Martialia hyadesi

Node 4 Nototodarus hawaiiensis

1.0 Todarodes pacificus

1.0 Nototodarus sloanii 1.0 Nototodarus gouldi

0 . 0 3

Fig. 1. Molecular phylogeny of the Ommastrephidae, and reconstructions of ancestral character states. Pie charts represent the median posterior probability of each spawning type for the common ancestor. Black, coastal spawning; Grey, oceanic spawning. Node values are the posterior probability of Bayesian analysis. Bars represent substitution/sites ratio along the branches.

HPD 95%) during the Miocene. Todarodinae (Clade 6). 68.7 Mya HPD and with better node support due to the markers used, and due that it 51.6–87.7. performed with Bayesian inference (Fig. 1). The three monophyletic The ancestral reconstruction analysis showed high posterior prob- clades corresponding to the three subfamilies traditionally described abilities (PP = 0.71) of having coastal spawning as the ancestral trait based on morphology (Illicinae, Ommastrephinae, Todarodinae) (e.g. (Node 1) (Table 1, Fig. 1). Species from the Subfamily Illicinae + To- Roeleveld, 1988; Wormuth, 1998). It has been proposed to place Or- daropsis eblanae (Node 2) would have maintained the ancestral coastal nithoteuthis on a fourth subfamily, Ornithoteuthinae, based on the strategy (PP = 0.81), while the Subfamily Ommastrephinae (Node 3) presence of intestinal and ocular photophores, unlike the rest of To- evolved to an oceanic strategy (PP = 0.98). Species from the Subfamily darodinae (Nigmatullin, 1979, 2007). Our results do neither support Todarodinae (Node 4) evolved to coastal strategy (PP = 0.91; Fig. 1). the placement of Ornithoteuthis in a separate subfamily (compare The kappa value was close to 1, suggesting a gradual evolution mode of Nigmatullin, 1979) nor in the Ommastrephinae, and instead confirms a the rate of change of both spawning types (κ = 1.08, HPD 95% closer relationship with the Todarodinae as previously found by 0.37–1.90, BF = 0.37). Wakabayashi et al. (2012). Moreover, our results show that the species Todaropsis eblanae is a sister group of Illicinae (Fig. 1). In a previous study using allozyme, T. eblanae was already been found outside the 4. Discussion subfamily Todarodinae (Yokawa, 1994), where T. eblanae it is tradi- tionally placed into. The placement of Todaropsis in a separate sub- The phylogenetic reconstruction obtained in the present study re- family Todaropsinae has been proposed due to differences in morpho- presents the three subfamilies previously found in other molecular logical traits (Nigmatullin, 2000). Following the diagnosis of studies (Yokawa, 1994; Wakabayashi et al., 2012), plus Todaropsinae,

214 M.C. Pardo-Gandarillas et al. Molecular Phylogenetics and Evolution 120 (2018) 212–217

Vampyroteuthis infernalis Argonauta nodosa 1.0 Hapalochlaena maculosa 1.0.0 Adelieledone polymorpha CP 2 0.95 1.0 Enteroctopus dofleini Spirula spirula CP 1 Sepia officinalis 1.0 Sepia pharaonis 1.0 1.0 1.0 Sepia elegans 0.95 Sepioteuthis lessoniana CP 4 Doryteuthis pleii Brazil 1.0 1.0 Doryteuthis pleii USA

1.0 Doryteuthis pealei CP 3 1.0 Doryteuthis opalescens 1.0 Watasenia scintillans

1.0 Bathyteuthis abyssicola Onychoteuthis banksii Onykia robusta 1.0 1.0 Onykia carriboea 1.0 1.0 Architeuthis dux Gonatus madokai 1.0 1.0 Gonatus fabricii Hyaloteuthis pelagica Clade 2 Eucleoteuthis luminosa 1.0 1.0 Sthenoteuthis oualaniensis 0.94 1.0 Sthenoteuthis pteropus Ommastrephinae

0.96 Ommastrephes bartramii

Clade 1 0.99 Dosidicus gigas Todaropsis eblanae 1.0 Clade 4 Todaropsinae Illex argentinus 0.97 Clade 5 Illex coindetii Illicinae 1.0 1.0 Illex illecebrosus Ornithoteuthis antillarum Clade 3 1.0 Ornithoteuthis volatilis

1.0 Todarodes filippovae

1.0 Martialia hyadesi 1.0 Todarodinae Clade 6 Nototodarus hawaiiensis Todarodes pacificus 1.0 Nototodarus gouldi 1.0 1.0 Nototodarus sloanii

250 200 150 100 50 0 Divergence times (Mya)

Fig. 2. Molecular divergence times of the Ommastrephidae. Bars in each node represent High Posterior Density 95%. CP 1: Calibration point 1 236 Mya, CP 2: Calibration point 2 182 Mya, CP 3: Calibration point 3 48 Mya, CP 4: Calibration point 4 16 Mya. Light blue box indicates the Ommastrephidae.

Table 1 smooth funnel groove (without foveola nor side pockets). However, T. Median posterior probabilities for the reconstruction of ancestral spawning types in eblanae differs from Illicinae in having four rows of suckers in the ommastrephid squids, as shown in Fig. 1 (HPD 95% range in parentheses). dactylus tentacle, instead of eights rows (Nigmatullin, 2000, 2007). Our

P (0) P (1) results are consistent with this, and support the placement of T. eblanae in the separate subfamily Todaropsinae, as proposed by Nigmatullin Node 1 0.71 (0.41–1.00) 0.29 (0.01–0.69) (2000). In addition, the genus Todarodes was found to be polyphyletic – – Node 2 0.81 (0.54 1.00) 0.19 (0.05 0.25) (Fig. 1), as well in previous attempts to reconstruct the family phylo- Node 3 0.02 (0.01–0.23) 0.98 (0.76–1.00) geny. In particular, T. pacificus was found inside the Nototodarus clade Node 4 0.91 (0.79–1.00) 0.09 (0.00–0.11) with high node support. The same phylogenetic position has been found P(0), coastal spawning; P(1), oceanic spawning. by Yokawa (1994) and Wakabayashi et al. (2012). These results high- light the need of a revision of genus Todarodes. In this study, 18 out of Nigmatullin (2000), T. eblanae differs from Todarodinae and Ommas- 22 ommastephid species (see Table S1) help to better resolve their trephinae in the structure of the funnel groove and the lack of photo- phylogenetic relationships. The missing species in this study include phores. At the same time, it differs from all other ommastrephids in three members of the genus Todarodes, and one of Illex (i.e. T. ango- having both abdominal arms hectocotylized, and in the gladius, which lensis, T. pusillus, T. sagittatus and I. oxygonius). In order to solve the is large at its cone, and wide and round in cross section (Nigmatullin, particular position of some species (T. pacificus, T eblanae) and the 2000). Todaropsis eblanae and Illex (Illicinae) share the trait of having a genus Ornithoteuthis, it is necessary to employ additional molecular

215 M.C. Pardo-Gandarillas et al. Molecular Phylogenetics and Evolution 120 (2018) 212–217 markers. (Tanner et al., 2017). These events could have favored a squid migra- Historically, our results point to a Late Jurassic origin (∼148 Mya) tion during the late Cretaceous and early Paleogene from continental for the Decapodiformes and a Late Cretaceous origin (∼87 Mya) for the shelf to oceanic waters, with squid seeking habitat and food opportu- Ommastrephidae. These divergence times are consistent with the only nities and gradually changing location and spawning type. In his hy- reliable evidence about the existence of teuthids based on Upper pothesis, Nigmatullin (1979, 2007) proposed that changes occurred Cretaceous beaks from Japan (Tanabe et al., 2015), and the molecular early in the Oligocene (∼33 Mya) when the sea temperature and sea estimations made by Tanner et al. (2017). Our results predate divergent level decreased drastically and scombrids radiated into oceanic waters. times previously proposed by Nesis (1978, 2003) and Nigmatullin Furthermore, there is evidence that these habitat shifts have been as- (2007) in which it was suggested that recent cephalopod fauna was sociated with rapid evolution in morphological, behavioral, and bio- formed during the Oligocene to Miocene (∼23 Mya). Additionally, our chemical traits in response to new environments (McPeek, 2000; Raia results contrast with older divergence times (around 179–271 Mya) et al., 2012). estimated by Strugnell et al. (2006), who used a Plesioteuthis fossil from By utilizing evidence from extant taxa and their phylogenetic re- Upper Jurassic (151 Mya) to calibrate the split between Ommas- lationships, in combination with new tools, it is now possible to in- trephidae and other oegopsids. Previous studies have suggested that vestigate evolutionary patterns of traits in the absence of a strong fossil squid–like Jurassic coleoids, such as Plesioteuthidae (Lower Jurassic – record (e.g. behavior, reproductive strategies), and a re-evaluation of Upper Cretaceous, 182–65 Mya) were the ancestors of modern om- old hypotheses on phylogenetically related species that have never been mastrephids, based on a similar gladius outline (Bizikov, 2008). How- tested statistically, improving the estimation dates of when this habitat ever, other studies have demonstrated that plesioteuthids belong to the change happened. Octopodiformes clade (e.g. Fuchs et al., 2007) with the squid–like ap- pearance of Jurassic–Cretaceous coleoids, and more likely attributed to Acknowledgments convergent evolution. Our analyses suggest an origin of the Ommas- trephidae preceding the Middle Eocene statolith fossils found for the This work was funded by grant FONDECYT 3110152. We would like group (Neige et al., 2016). These fossils could not be used for our ca- to thank Ian Gleadall and Daniela Silva Gandarillas for comments that librations, since it is not clear which subfamilies they belong to. Other significantly improved the manuscript. We are grateful to João Bráullio ommastrephid fossil statoliths from Oligocene (5.3 Mya, Neige et al., de Luna Sales for providing sequences of Doryteuthis pleii from USA and 2016) are evidence of the existence of Dosidicus and Sthenoteuthis Brazil. genera during Paleogene. It is necessary to exercise caution as con- flicting classifications of cephalopod fossils have produced inconsistent Appendix A. Supplementary material divergence times, and thus conflicting conclusions about cephalopod evolution (see Kröger et al., 2011; Neige et al., 2016). Supplementary data associated with this article can be found, in the The reconstruction of the ancestral spawning type suggests that online version, at https://doi.org/10.1016/j.ympev.2017.12.014. early ommastrephid squids inhabited and spawned in coastal waters, with some species colonized the open ocean, evolving an oceanic References spawning strategy, as seen in the subfamily Ommastrephinae and some species of the subfamily Todarodinae. Other groups may have kept the Bizikov, V.A., 2008. Evolution of the Shell in Cephalopoda. VNIRO Publishing, Moscow, ancestral coastal spawning, such as the genus Illex which experienced a pp. 447. fi fi ∼ Davis, M.P., Holcroft, N.I., Wiley, E.O., Sparks, J.S., Smith, W.L., 2014. Species-speci c recent diversi cation during the Lower Miocene ( 16.5 Mya). Our bioluminescence facilitates speciation in the deep sea. Mar. Biol. 161, 1139–1148. results statistically support the ancestral coastal spawning hypothesis Dynesius, M., Jansson, R., 2000. 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