Heterochronic Developmental Shift Caused by Thyroid Hormone in Larval Sand Dollars and Its Implications for Phenotypic Plasticity and the Evolution of Nonfeeding Development

Abstract

Abstract. Recent work on a diverse array of echinoderm species has demonstrated, as is true in amphibians, that thyroid hormone (TH) accelerates development to metamorphosis. Interestingly, the feeding larvae of several species of sea urchins seem to obtain TH through their diet of planktonic algae (exogenous source), whereas nonfeeding larvae of the sand dollar Peronella japonica produce TH themselves (endogenous source). Here we examine the effects of TH (thyroxine) and a TH synthesis inhibitor (thiourea) on the development of Dendraster excentricus, a sand dollar with a feeding larva. We report reduced larval skeleton lengths and more rapid development of the juvenile rudiment in the exogenous TH treatments when compared to controls. Also, larvae treated with exogenous TH reached metamorphic competence faster at a significantly reduced juvenile size, representing the greatest reduction in juvenile size ever reported for an echinoid species with feeding larvae. These effects of TH on D. excentricus larval development are strikingly similar to the phenotypically plastic response of D. excentricus larvae reared under high food conditions. We hypothesize that exogenous (algae-derived) TH is the plasticity cue in echinoid larvae, and that the larvae use ingested TH levels as an indicator for larval nutrition, ultimately signaling the attainment of metamorphic competence. Furthermore, our experiments with the TH synthesis inhibitor thiourea indicate that D. excentricus larvae can produce some TH endogenously. Endogenous TH production might, therefore, be a shared feature among sand dollars, facilitating the evolution of nonfeeding larval development in that group. Mounting evidence on the effects of thyroid hormones in echinoderm development suggests life-history models need to incorporate metamorphic hormone effects and the evolution of metamorphic hormone production.

Biochemical Mechanisms of Thyroid Hormone Deiodination

“…The tree resolved into four main clusters containing the three vertebrate deiodinase subtypes, with the invertebrate deiodinases forming a seperate cluster, branching close to the origin of the tree. All in all there is now sound evidence that the iodothyronine deiodinases as well as TRs arose in a urochordate, or perhaps even earlier in evolution since iodothyronines have effects on echinoderms (27,30) such as sea urchins and sand dollars. This indicates that iodothyronines and possibly TRs and deiodinases arose earlier in evolution than receptors for gender/adrenal steroids and steroid-synthesizing enzymes.…”

An iodothyronine deiodinase from Chlamys farreri and its induced mRNA expression after LPS stimulation

“…Thyroid hormones are released by the thyroid gland or immunocytes after immune stimulation to bind thyroid hormone receptors located in immunocytes to regulate the expression of the immune-related genes in vertebrates [9]. Thyroid hormones have also been detected in some invertebrates, such as echinoid and anthozoan [10]. There are abundant evidence to support that thyroid hormones could modulate metamorphose and development of invertebrates [10,11].…”

“…Thyroid hormones have also been detected in some invertebrates, such as echinoid and anthozoan [10]. There are abundant evidence to support that thyroid hormones could modulate metamorphose and development of invertebrates [10,11]. However, the modulation of thyroid hormones to the immune response is far from well understood [12,13].…”

The amphioxus genome enlightens the evolution of the thyroid hormone signaling pathway

“…Not much is known about the TH pathways of non-vertebrate chordates (the vertebrate sister group urochordates like the sea squirt Ciona intestinalis, and the cephalochordates like amphioxus), except that they possess an organ homologous to the thyroid gland, which is named endostyle, and can produce THs (see Paris and Laudet 2008 for a review). However, biological effects of THs outside vertebrates have been reported several times, and THs have been linked with metamorphosis in urochordates (Patricolo et al 2001), amphioxus , and in echinoderms (Heyland and Hodin 2004).…”