Anatomical and molecular reinvestigation of lamprey endostyle development provides new insight into thyroid gland evolution

Abstract

The thyroid gland of vertebrates is considered to be homologous to the endostyle of non-vertebrate chordates (cephalochordates, urochordates), a key character for understanding the origin and evolution of the chordate body plan. In lampreys, the larval endostyle transforms into an adult thyroid gland during metamorphosis, reflecting evolutionary changes that occurred in the vertebrate lineage. Focussing on thyroid-like cells in the endostyle, we here relate morphologically visible steps of lamprey (Lampetra fluviatilis) endostyle differentiation to embryonic stages and determine the onset of thyroid-like function. Analysing lamprey endostyle development using semi-thin histological sections, immunohistochemical detection of thyroid hormone, and the molecular marker thyroid transcription factor1 (Ttf1) refines our current view of the homology between endostyle and thyroid gland. In contrast to earlier literature, we find that a duct always persists to connect the endostyle lumen to the pharynx, a structure that resembles the thyroglossal duct in thyroid development and could further support the homology between endostyle and thyroid. Before the onset of thyroid-like function, Ttf1 expression becomes restricted to the ventral part of the endostyle, on the one hand showing that dorsal thyroid-like cells produce thyroid hormone in the absence of Ttf1, and on the other suggesting that Ttf1 was initially involved in specifying ventral fates in the endostyle.

Iodothyronine deiodinases: a functional and evolutionary perspective

“…Indeed, current information supports the notion that the vertebrate thyroid gland, as well as the endostyle and subpharyngeal gland in invertebrate chordates, may have evolved from a common ancestor (for review Kluge et al (2005) and Paris et al (2008)). Thus, the genomes of cephalochordates (amphioxus) and urochordates (tunicates) contain orthologs of the main genes involved in thyroid hormonogenesis and the TH-signaling pathway (Na/I symporter, thyroid peroxidase, deiodinase, and TH receptor), but they lack the components for neuroendocrine control of the thyroid (for review : Holland et al (2008) and Paris et al (2008)).…”

Development of the thyroid gland

“…Intriguingly, the larval endostyle in lampreys metamorphoses into a follicular thyroid (Fig. 2D), thus representing a transitional phase in thyroid evolution towards an endocrine gland (Marine, 1913;Wright and Youson, 1976;Kluge et al, 2005).…”

The history of a developmental stage: Metamorphosis in chordates

“…It is the mucus nonproducing, smallest, most dorsal and posterior part that is thought to be the homologue of the thyroid follicles. This hypothesis was based on several arguments: (i) the endostyle and the thyroid gland are located in a similar position in the body plan, (ii) some endostyle cells have thyroid-producing properties such as iodine uptake (Fredriksson et al, 1985;Manzon and Youson, 2002;Thomas, 1956) and TH metabolism (Barrington and Thorpe, 1968;Covelli et al, 1960;Kluge et al, 2005;Manzon and Youson, 2002), (iii) several thyroid-specific genes are expressed during endostyle formation [Ttf1 in lamprey (Kluge et al, 2005)], and (iv) in lamprey, some cells of the endostyle transform into thyroidal follicles during metamorphosis (Fredriksson, 1988).…”