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The anatomy of the jawless fish head and the early evolution of vertebrates

Tetsuto Miyashita

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Abstract

No other structure better characterizes vertebrates than the head, with its intricate nervous innervations, highly specialized muscles, and massive skull. Did the first vertebrate possess all of those traits, or did early vertebrates acquire them in steps? Answers may lie in the jawless grade of vertebrates. Based on dissections, a histological analysis, and μCT imaging of cartilages, muscles, and nerves in hagfish and lampreys, I demonstrate that the biomechanics of jawless vertebrate head differs from that of jawed vertebrates in two distinct ways: linear muscle antagonism and elastic recoiling of the skeleton. I report structures in both hagfish and lampreys that either represent precursors to jawed vertebrate conditions (e.g., cardinal heart foreshadowing synovial joints; replacement of tooth plates mimicking that of the true teeth) or appear to be intermediate between two distinct tissues of jawed vertebrates (e.g., a cartilage functionally acting as a skeletal element but histologically identical to tendons). Evolutionary precursors to the jawed vertebrate conditions appeared in steps and transformed quickly at the origin of jaws. Coupled with the molecular genetic evidence, I present an evolutionary scenario for early vertebrates in which expression of the mandibular‐patterning Dlx pathway shifts via a series of specializations in feeding and respiratory structures. Grant Funding Source : NSERC

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No other structure better characterizes vertebrates than the head, with its intricate nervous innervations, highly specialized muscles, and massive skull. Did the first vertebrate possess all of those traits, or did early vertebrates acquire them in steps? Answers may lie in the jawless grade of vertebrates. Based on dissections, a histological analysis, and μCT imaging of cartilages, muscles, and nerves in hagfish and lampreys, I demonstrate that the biomechanics of jawless vertebrate head differs from that of jawed vertebrates in two distinct ways: linear muscle antagonism and elastic recoiling of the skeleton. I report structures in both hagfish and lampreys that either represent precursors to jawed vertebrate conditions (e.g., cardinal heart foreshadowing synovial joints; replacement of tooth plates mimicking that of the true teeth) or appear to be intermediate between two distinct tissues of jawed vertebrates (e.g., a cartilage functionally acting as a skeletal element but histologically identical to tendons). Evolutionary precursors to the jawed vertebrate conditions appeared in steps and transformed quickly at the origin of jaws. Coupled with the molecular genetic evidence, I present an evolutionary scenario for early vertebrates in which expression of the mandibular‐patterning Dlx pathway shifts via a series of specializations in feeding and respiratory structures. Grant Funding Source : NSERC

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Available abstract

No other structure better characterizes vertebrates than the head, with its intricate nervous innervations, highly specialized muscles, and massive skull. Did the first vertebrate possess all of those traits, or did early vertebrates acquire them in steps? Answers may lie in the jawless grade of vertebrates. Based on dissections, a histological analysis, and μCT imaging of cartilages, muscles, and nerves in hagfish and lampreys, I demonstrate that the biomechanics of jawless vertebrate head differs from that of jawed vertebrates in two distinct ways: linear muscle antagonism and elastic recoiling of the skeleton. I report structures in both hagfish and lampreys that either represent precursors to jawed vertebrate conditions (e.g., cardinal heart foreshadowing synovial joints; replacement of tooth plates mimicking that of the true teeth) or appear to be intermediate between two distinct tissues of jawed vertebrates (e.g., a cartilage functionally acting as a skeletal element but histologically identical to tendons). Evolutionary precursors to the jawed vertebrate conditions appeared in steps and transformed quickly at the origin of jaws. Coupled with the molecular genetic evidence, I present an evolutionary scenario for early vertebrates in which expression of the mandibular‐patterning Dlx pathway shifts via a series of specializations in feeding and respiratory structures. Grant Funding Source : NSERC

Key concepts: Hagfish, Vertebrate, Biology, Anatomy, Evolutionary biology, Gene, Biochemistry

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