SHORT COMMUNICATION

Juvenile morphology in baleen whale phylogeny

Cheng-Hsiu Tsai & R. Ewan Fordyce

Received: 10 June 2014 /Revised: 2 July 2014 /Accepted: 21 July 2014 /Published online: 1 August 2014# Springer-Verlag Berlin Heidelberg 2014

Abstract Phylogenetic reconstructions are sensitive to theinfluence of ontogeny on morphology. Here, we use foetal/neonatal specimens of known species of living baleen whales(Cetacea: Mysticeti) to show how juvenile morphology ofextant species affects phylogenetic placement of the species.In one clade (sei whale, Balaenopteridae), the juvenile isdistant from the usual phylogenetic position of adults, but inthe other clade (pygmy right whale, Cetotheriidae), the juve-nile is close to the adult. Different heterochronic processes atwork in the studied species have different influences on juve-nile morphology and on phylogenetic placement. This studyhelps to understand the relationship between evolutionaryprocesses and phylogenetic patterns in baleen whale evolutionand, more in general, between phylogeny and ontogeny; like-wise, this study provides a proxy how to interpret the phylog-eny when fossils that are immature individuals are included.Juvenile individuals in the peramorphic acceleration cladeswould produce misleading phylogenies, whereas juvenile in-dividuals in the paedomorphic neoteny clades should stillprovide reliable phylogenetic signals.

Keywords Evolutionary process . Phylogenetic pattern .

Ontogeny .Mysticeti . Heterochrony

Introduction

Ever since Darwin (1859), it has been clear that patterns ofrelationship are fundamentally linked to the process of

evolution (Stanley 1979; Eldredge and Cracraft 1980). Pat-terns of phylogeny are the foundation for interpretations andperceptions of the biological world. Equally, it is important tounderstand evolutionary processes and to help interpret theorigin andmeaning of phylogenetic patterns. A previous study(Tsai and Fordyce 2014) considered the influence of differentheterochronic evolutionary processes in a clade of baleenwhales (Cetacea: Mysticeti). We now consider the influenceof juvenile morphology on phylogenetic reconstruction. Juve-nile morphology can hamper understanding of relationships,especially amongst fossils. Examples for dinosaurs include thesynonymy of Torosaurus, which was based on juvenile mate-rial, with Triceratops (see Scannella and Horner 2010;Longrich and Field 2012), and the identity of the hadrosauridGlishades ericksoni (Prieto-Marquez 2010) that was laterinterpreted as an indeterminate juvenile hadrosaurid(Campione et al. 2013). Here, we include juvenile baleenwhale specimens of known identity, but generalised structurein phylogenetic analyses in which species-level morphologiesare expressed clearly.

Material and methods

Two young (foetus/neonate) and well-preserved baleen whalespecimens are used as separate operational taxonomic units(OTUs) and incorporated into the two phylogenetic matricesof Fordyce and Marx (2013) and Bisconti et al. (2013). Toallow ready comparison with published results, we did notchange or modify any coding of the adult Caperea andBalaenoptera in the two published matrices. Codings there-fore involved 166 and 246 morphological characters forBalaenoptera borealis (NSMT M24943, skull length:42.5 cm) and Caperea marginata (SAMM9079, skull length:50.3 cm). Globally, well-preserved foetal/neonatal specimenssuitable for full phylogenetic coding are extremely rare, aselaborated earlier (Tsai and Fordyce 2014); the specimens

Communicated by: Sven Thatje

Electronic supplementary material The online version of this article(doi:10.1007/s00114-014-1216-9) contains supplementary material,which is available to authorized users.

C.<H. Tsai (*) : R. E. FordyceDepartment of Geology, University of Otago, Dunedin, New Zealande-mail: cheng-hsiu.tsai@otago.ac.nz

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coded here were the only two suitable from major collec-tions in Japan and Australia. Details of specimens, includ-ing photos, and discussion of the age determination inbaleen whales are in a supplementary file (S1). The twodata matrices (Fordyce and Marx 2013; Bisconti et al.2013) used in this study represent different selections offossil and modern mysticete taxa and different interpreta-tions of homology for some characters. The use of twodifferent matrices helps to better identify the role ofjuvenile morphology in phylogenetic analyses. In summa-ry, the analyses used TNT to perform a heuristic parsimo-ny analysis (Goloboff et al. 2003, 2008); details are in asupplementary file (S2).

Results

Results from both analyses for each foetal/neonatal animalshow a consistent phylogenetic position (Figs. 1 and 2): youngB. borealis (NSMT M24943) lies far from the familyBalaenopteridae within which B. borealis actually belongs,whereas young C. marginata (SAM M9079) lies in the cladethat also contains adult C. marginata. Specifically:

1. B. borealis NSMTM24943 plots in two positions remotefrom adult B. borealis:

(a) B. borealis forms a clade with the Balaenidae (rightwhales) according to Fordyce and Marx (2013) or

(b) B. borealis is in the most basal lineage of the crownMysticeti according to Bisconti et al. (2013).

2. C. marginata SAM M9079 falls in the same lineage asadult C. marginata:

(a) C. marginata is in the Cetotheriidae as a sister taxonto adult C. marginata, though with high morpholog-ical disparity as shown by branch length according toFordyce and Marx (2013) or

(b) C. marginata is the most basal member of theBalaenoidea (adult C. marginata and right whales)according to Bisconti et al. (2013).

Details of the cladograms and morphological charactersthat support the clades of those two foetal/neonatal specimensare in a supplementary file (S2).

Discussion

The contrasting phylogenetic positions of B. borealis andC. marginata (Figs. 1 and 2) show that juvenile morphologiesmay greatly influence phylogenetic reconstructions. The na-ture and degree of morphological change during ontogeny

produce quite different phylogenies for the two baleen whalefamilies, Balaenopteridae and Cetotheriidae. Previously, thedisparate skull ontogenies in B. borealis and C. marginatawere analysed qualitatively and quantitatively (using geomet-ric morphometrics) to show that different heterochronic pro-cesses operate in the two lineages. Peramorphic acceleration,which consists of an increase in the rate of morphologicaldevelopment during ontogeny, is involved for B. borealis.Conversely, paedomorphic neoteny, which reduces the rateof morphological development during the juvenile phase,resulting in a morphologically “retarded” adult occurs inC. marginata (Tsai and Fordyce 2014). Heterochronic pro-cesses such as these are important and widely recognisedmechanisms in evolutionary history, involving morphologicalchanges in many clades (Gould 1977; McKinney 1988; Mc-Namara 1995). Since evolutionary heterochrony results in awide range of morphological modification, the effects ofheterochronic processes on phylogenetic reconstructions canbe complex and profound, potentially misleading interpreta-tion (e.g. heterochronic paedomorphism in salamanders;Wiens et al. 2005). Here, different heterochronic processesin different lineages have quite different influences on phylo-genetic reconstructions: peramorphic acceleration inB. borealis results in phylogenetic disparities between juvenileand adult specimens, whereas paedomorphic neoteny inC. marginata mitigates the phylogenetic incongruence acrossdifferent ontogenetic stages.

Phylogenetic pattern and evolutionary process in baleenwhales

Research on the phylogeny of the world’s largest animals(baleen whales) has grown fast. Many recent contributionson mysticete phylogeny involve new interpretations ofbroader patterns (Fordyce and Marx 2013), analyses usinglarge data matrices (Steeman 2007; Marx 2011; Biscontiet al. 2013), and descriptions of many new species. Forexample, supplementary file S3 lists 44 living and fossilbaleen whale species named or re-described since 2000. Ofnote is the debate on the phylogenetic position ofC. marginata, which was recognised as a cetotheriid byFordyce and Marx (2013) and Marx et al. (2013), but as abalaenoid by Bisconti (2014) and El Adli et al. (2014). Suchvariation in phylogenetic placement reflects the use of bothdifferent morphological datasets and different interpretationsof morphological homologies. Homology is clearly a funda-mental issue in comparative biology (Hall 1994) and has longbeen the foundation of cetacean morphology, function, sys-tematics, and phylogeny (Mead and Fordyce 2009, and refer-ences therein). Nevertheless, the evolutionary processes thatproduce morphologically disparate homologues in closelyrelated baleen whales have been discussed little. Tsai and

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Fig. 1 Phylogenetic positions offoetal B. borealisNSMTM24943and foetal/neonatal C. marginataSAM M9079 using the matrix ofFordyce and Marx (2013). FoetalB. borealis (rorqual,Balaenopteridae) plots as a basalbalaenid; foetal/neonatalC. marginata SAMM9079 formsa sister taxon with adultC. marginata with highmorphological disparity. Thenumber above each branchindicates how many characterschange, leading to each taxonfrom the node. Details about thecladogram are in S2. Bottom leftshows a stillborn C. marginataNMNZ MM2959. Daggerindicates extinct species. Plei.Pleistocene Holo. Holocene

Fig. 2 Phylogenetic positions(strict consensus of 48 trees) offoetal B. borealisNSMTM24943and foetal/neonatal C. marginataSAM M9079 using the matrix ofBisconti et al. (2013). FoetalB. borealis (rorqualBalaenopteroidea) wasrecognised as a basal taxon to thecrown Mysticeti; foetal/neonatalC. marginata is the basal taxon tothe Balaenoidea, but still in thesuggested clade. The numberabove each branch indicates howmany characters change, leadingto each taxon from the node; formore information about thecladogram, refer to S2. Daggerindicates extinct species. Plei.Pleistocene Holo. Holocene

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Fordyce (2014) identified two different heterochronic pro-cesses in baleen whale evolution based on ontogenetictrajectories deduced from the study of skulls of differentontogenetic age.

Pattern and process are deeply intertwined in evolution(Stanley 1979; Eldredge and Cracraft 1980). Macro-evolutionary processes are often inferred from phylogeneticpatterns amongst neospecies (Mooers and Heard 1997; Pagel1997), yet a wide understanding of macro-evolutionary pro-cesses relies on a foundation of abundant and/or well-sampledfossils (e.g. Eldredge and Gould 1972). Although perhaps95 % of species from evolutionary history no longer exist(Nee and May 1997), the record of baleen whale history isburgeoning, thanks to the recent research on living and espe-cially fossil baleen whales (see supplementary file S3). Ideal-ly, interpretation of evolutionary processes would be based onthe study of morphological change in actual ancestor–descen-dant sequences, a situation rarely achieved. Most studies mustuse a patchy record. For example, in mysticete evolution, theOligocene aetiocetids are considered as bridging the morpho-logical gap between archaic toothed stem Cetacea and latertoothless baleen whales (Deméré et al. 2008; Fitzgerald 2012),yet details of species-level successions in this major evolu-tionary transition are unknown. Other toothed mysticetes inthe families Llanocetidae (Eocene) and Mammalodontidae(Oligocene) have equally problematic histories, with themammalodontids representing a relict and possibly paedo-morphic lineage (Fitzgerald 2010). The role of heterochronymay have been an important mechanism to produce novelmorphologies, such as seen in the robust-toothed putativemysticete Janjucetus or the walrus-mimic dolphinOdobenocetops (see Fitzgerald 2006; de Muizon 1993). Thisstudy shows that juvenile morphology may seriously influ-ence phylogenetic placements of Balaenopteridae andCetotheriidae, helping to understand how heterochronic evo-lutionary processes and phylogenetic patterns are associated.To date, the distribution of heterochronic processes in fossiland living baleen whales remains poorly understood. It isdesirable to elucidate detailed heterochronic processes acrossspecies/lineages and decipher how evolutionary process andphylogenetic pattern are linked.

Acknowledgments For access to collections and allowing photographyduring Tsai’s and/or Fordyce’s visits, we thank Tadasu Yamada, NaokiKohno, Yuko Tajima (National Museum of Nature and Science, Tokyo,Japan), Catherine Kemper, David Stemmer, Neville Pledge, Mary-AnneBinnie (South Australian Museum, Adelaide, Australia), James Mead,Charles Potter, John Ososky, Nicholas Pyenson, David Bohaska (Nation-al Museum of Natural History, Smithsonian Institution, Washington DC,USA), Jim Dines, David Janiger (Natural History Museum, of LosAngeles County, USA), Anton van Helden (National Museum of NewZealand, Wellington, New Zealand), and Erich Fitzgerald, Karen Roberts(Museum Victoria, Melbourne, Australia). We thank Gabriel Aguirre,Felix Marx, and Erich Fitzgerald for the review and comments; RobertBoessenecker and Yoshihiro Tanaka for the discussion. We thank Olivier

Lambert, Erich Fitzgerald, and an anonymous reviewer for their construc-tive comments. James Mead (Washington DC), Erich Fitzgerald, KarenRoberts (Melbourne), and Felix Marx, Ikerne Aguirre, Aiko Fukumoto(Japan) kindly accommodated Tsai during various visits. This study ispart of Tsai’s Ph.D. thesis supported by the University of Otago DoctoralScholarship.

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