Disconnecting Bones Within the Jaw‐Otic Network Modules Underlies
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Journal of Anatomy J. Anat. (2019) 235, pp15--33 doi: 10.1111/joa.12992 Disconnecting bones within the jaw-otic network modules underlies mammalian middle ear evolution Aitor Navarro-Dıaz,1 Borja Esteve-Altava2 and Diego Rasskin-Gutman1 1Paleobiology and Theoretical biology (Theoretical Biology), Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Valencia, Spain 2Institute of Evolutionary Biology (UPF-CSIC), Department of Experimental and Health Sciences, University Pompeu Fabra, Barcelona, Spain Abstract The origin of the mammalian middle ear ossicles from the craniomandibular articulation of their synapsid ancestors is a key event in the evolution of vertebrates. The richness of the fossil record and the multitude of developmental studies have provided a stepwise reconstruction of this evolutionary innovation, highlighting the homology between the quadrate, articular, pre-articular and angular bones of early synapsids with the incus, malleus, gonial and ectotympanic bones of derived mammals, respectively. There are several aspects involved in this functional exaptation: (i) an increase of the masticatory musculature; (ii) the separation of the quadrate bone from the cranium; and (iii) the disconnection of the post-dentary bones from the dentary. Here, we compared the jaw-otic complex for 43 synapsid taxa using anatomical network analysis, showing that the disconnection of mandibular bones was a key step in the mammalian middle ear evolution, changing the skull anatomical modularity concomitant to the acquisition of new functions. Furthermore, our analysis allows the identification of three types of anatomical modules evolving through five evolutionary stages during the anatomical transformation of the jawbones into middle ear bones, with the ossification and degradation of Meckel’s cartilage in mammals as the key ontogenetic event leading the change of anatomical modularity. Key words: anatomical network analysis (AnNA); Meckel’s cartilage; modularity; synapsida. – Introduction (Watson, 1953; Hopson, 1966; Carroll, 1988, chapters 17 18; Rubidge & Sidor, 2001; Sidor, 2001, 2003; Luo, 2011; Han Several structures of the middle ear of mammals evolved et al., 2017; Luo et al., 2017) and recent advances in devel- from the lower jaw of basal synapsids through a series of opmental biology (Luo, 2011; Anthwal et al., 2013, 2017; anatomical changes that started about 315 million years Ramırez-Chaves et al., 2016; Urban et al., 2017). ago. The now extinct non-mammal synapsids had a lower The origin of the mammalian middle ear goes back to the jaw made of up to eight bones, which articulated to the mandibular and jaw joint arrangement of primitive synap- rest of the skull through the articular-quadrate jaw joint; sids. According to the Reichert–Gaupp theory, based on their only auditory bone was the stapes (Crompton & Par- comparative anatomy and development, the ectotympanic, ker, 1978; Sidor, 2003; Meng et al., 2011; Urban et al., gonial, malleus and incus bones of the ear in mammals are 2017). In contrast, modern mammals have a single jawbone, homologous to the angular, pre-articular, articular and the dentary, which articulates to the squamosal, and four quadrate bones of the jaw in reptiles (Rich et al., 2005; Luo, closely connected auditory bones: ectotympanic, malleus, 2011; Meng et al., 2011; Maier & Ruf, 2016; Han et al., incus and stapes. Many aspects of the origin and evolution 2017). At the same time, the evolutionary history of the of the mammalian middle ear are now better understood synapsid lower jaw suggests a trade-off between an thanks to the richness of the synapsids fossil record increase in the area of muscle attachment and a reduction of some mandibular bones to improve sound transmission (Hopson, 1966; Kermack et al., 1973; Fourie, 1974; Cromp- ton & Parker, 1978; Kemp, 1979, 2007; Carroll, 1988, pp. Correspondence 393–395; Wang et al., 2001; Sidor, 2003; Soares et al., 2011; Diego Rasskin-Gutman, Paleobiology and Theoretical Biology (Theo- retical Biology), Cavanilles Institute of Biodiversity and Evolutionary Ramırez-Chaves et al., 2016; Lautenschlager et al., 2017, Biology, University of Valencia, C/ Catedratico Jose Beltran n°2, 2018). During the Permian, synapsids evolved a new power- 46980 Paterna, Valencia, Spain. E: [email protected] ful adductor musculature attached to jawbones (Kemp, Accepted for publication 6 March 2019 1969, 1979; Reisz, 1972; Fourie, 1974; Crompton & Parker, Article published online 12 April 2019 1978). Such innovation enabled early synapsids to feed © 2019 Anatomical Society 16 Network modularity of the mammalian middle ear evolution, A. Navarro-Dıaz et al. larger preys and to increase their body mass (Watson, 1953; 2003; Kemp, 2007; Meng et al., 2011; Anthwal et al., 2013). Reisz, 1972; Carroll, 1988, pg. 363; Kammerer, 2011), leading The reduction in size and the cranial disconnection of this to an increase of the dentary surface that allowed the inser- bony chain increased its vibrational mobility and airborne tion of new-developed muscle fibers that changed biting sound sensitivity (Kermack et al., 1981; Laurin, 1998; Kemp, mechanisms (Carroll, 1988, p. 393; Lautenschlager et al., 2007; Luo, 2011; Meng et al., 2011). Mesozoic mammals 2017, 2018). evolved a new dentary-squamosal jaw joint (Hopson, 1966; After the Permian-Triassic and the Triassic-Jurassic mass Romer, 1970; Crompton & Parker, 1978; Luo & Crompton, extinction events, non-mammalian therapsids reduced their 1994; Kemp, 2007; Luo, 2011; Anthwal et al., 2013; Han body size (Hopson, 1966; Frobisch,€ 2007; Kemp, 2007; Sig- et al., 2017) and relocated the primitive quadrate-articular urdsen et al., 2012; Huttenlocker, 2014). The first small jaw joint to the middle ear after the novel ossification of an insectivorous mammaliaforms originated during the Triassic embryological mandibular element, the Meckel’s cartilage (Fourie, 1974; Carroll, 1988, pp. 401–402; Sidor, 2001) and (Wang et al., 2001; Meng et al., 2011; Urban et al., 2017). had a nocturnal lifestyle (Kermack et al., 1981; Luo, 2011; The loss of bones and the disconnections in the lower jaw Han et al., 2017). Living in the shadow of the large archo- (Sidor, 2001; Luo, 2011; Meng et al., 2011; Han et al., 2017; saurs that dominated this period, any anatomical changes Urban et al., 2017) produced novel patterns of anatomical on sensory organs that favored avoiding predation, as well organization in the jaw-otic complex. Authors recognize as detecting and capturing smaller prey, would have posed three distinct patterns of organization or configuration a selective advantage (Kermack et al., 1981; Luo, 2011; types in synapsids: (i) the mandibular middle ear type, with Urban et al., 2017). Triassic mammaliaforms had a fully reor- post-dentary bones attached to the dentary and a func- ganized musculoskeletal mandibular complex with some tional quadrate-articular jaw joint (Fig. 1A–D); (ii) the tran- jawbones having distinct new roles (Hopson, 1966; Kermack sitional mammalian middle ear type, with the middle ear et al., 1973; Kemp, 1979; Meng et al., 2011; Anthwal et al., bones indirectly connected to the mandible by a link to the 2013; Han et al., 2017; Lautenschlager et al., 2017, 2018). ossified Meckel’s cartilage (Fig. 1E); and (iii) the definitive Thereby, the enlarged dentary assumed all the masticatory mammalian middle ear type, with the middle ear bones muscular insertion in the new Mesozoic mammals, while fully disconnected from the dentary and isolated from par- the smaller post-dentary bones evolved an auditory role ticipating in any chewing action (Fig. 1F; Luo, 2011; Meng that improved sound transmission from the lower jaw to et al., 2011; Ramırez-Chaves et al., 2016; Anthwal et al., the inner ear through a bony chain between the angular, 2017; Han et al., 2017; Luo et al., 2017). These configura- articular, quadrate and stapes bones (Hopson, 1966; Ker- tions can also be seen as changes in the topological mack et al., 1973, 1981; Crompton & Parker, 1978; Sidor, arrangement of the ear bones throughout their evolution. Fig. 1 Representation of the lower jaw transition throughout the synapsid evolution. Notice the enlargement of the dentary bone, concomitant to the reduction of post-dentary bones until their disconnection as new mammalian middle ear bones. Lower jaws from (A) to (D) illustrate the mandibular middle ear type, with post-dentary bones fully attached to the dentary; the lower jaw arrangement of (E) illustrates the transitional mammalian middle ear type, with the ear bones indirectly connected to the dentary by the ossified Meckel’s cartilage; and (F) illustrates the defini- tive mammalian middle ear type, with the ear bones totally disconnected from the dentary bone. (A) Medial view of the lower jaw of the primitive synapsid Dimetrodon (modified from Sidor, 2003). (B) Medial view of the lower jaw of the gorgonopsian therapsid Aelurognathus (modified from Broom, 1913). (C) Medial view of the lower jaw of the cynognathian cynodont Diademodon (modified from Hopson, 1966). (D) Medial view of the lower jaw of the mammaliaform Morganucodon (modified from Kermack et al., 1973). (E) Medial view of the lower jaw of the eutriconodont mammal Yanoconodon (modified from Luo et al., 2007). (F) Lateral view of the lower jaw and middle ear bones of the marsupial mammal Mon- odelphis (Wible, 2003; Luo, 2011). Mandibles are not to scale. © 2019 Anatomical Society Network modularity of the mammalian middle ear evolution, A. Navarro-Dıaz