Developmental and genomic insight into the origin of the tardigrade body plan

Abstract

Tardigrada is an ancient lineage of miniaturized animals. As an outgroup of the well‐studied Arthropoda and Onychophora, studies of tardigrades hold the potential to reveal important insights into body plan evolution in Panarthropoda. Previous studies have revealed interesting facets of tardigrade development and genomics that suggest that a highly compact body plan is a derived condition of this lineage, rather than it representing an ancestral state of Panarthropoda. This conclusion was based on studies of several species from Eutardigrada. We review these studies and expand on them by analyzing the publicly available genome and transcriptome assemblies of Echiniscus testudo, a representative of Heterotardigrada. These new analyses allow us to phylogenetically reconstruct important features of genome evolution in Tardigrada. We use available data from tardigrades to interrogate several recent models of body plan evolution in Panarthropoda. Although anterior segments of panarthropods are highly diverse in terms of anatomy and development, both within individuals and between species, we conclude that a simple one‐to‐one alignment of anterior segments across Panarthropoda is the best available model of segmental homology. In addition to providing important insight into body plan diversification within Panarthropoda, we speculate that studies of tardigrades may reveal generalizable pathways to miniaturization.

Old hypotheses and theories at the heart of current evo‐devo research

“…The phylogenetic position of tardigrades, as well as the homology of some of their compact body plan, remain uncertain. Here, Smith et al (2023) argue that the loss of some of the iconic Hox genes in the tardigrade lineage accompanied the loss of ancestral trunk segments. They also examine the evolution of developmental genes involved, for instance, in leg patterning to decipher the evolution of the tardigrade body plan (Smith et al, 2023).…”

Expression patterns of FGF and BMP pathway genes in the tardigradeHypsibius exemplaris

“…Tardigrades comprise an entire phylum of animals whose development is little studied. Tardigrades are well positioned for studying the evolution of development of diverse organisms, as they are members of the diversely shaped ecdysozoan animals, a clade that also includes arthropods and nematodes (Aguinaldo et al, 1997; Gabriel et al, 2007; Smith et al, 2023). Tardigrades exhibit a body plan consisting of a head with two eyes and four leg-bearing trunk segments (reviewed in Schill, 2018).…”

“…Homology of major body regions of H. exemplaris embryos has been explored through the lens of Hox gene expression patterns (Smith et al, 2016). Patterning has been explored by studying proximal-distal leg patterning genes, nervous system patterning genes, and Engrailed and Pax3/7 (Gabriel and Goldstein, 2007; Game and Smith, 2020; Smith et al, 2023, 2018).…”