Functional genetic analysis in a jawless vertebrate, the sea lamprey: insights into the developmental evolution of early vertebrates

Abstract

Lampreys and hagfishes are the only surviving relicts of an ancient but ecologically dominant group of jawless fishes that evolved in the seas of the Cambrian era over half a billion years ago. Because of their phylogenetic position as the sister group to all other vertebrates ( jawed vertebrates), comparisons of embryonic development between jawless and jawed vertebrates offers researchers in the field of evolutionary developmental biology the unique opportunity to address fundamental questions related to the nature of our earliest vertebrate ancestors. Here, we describe how genetic analysis of embryogenesis in the sea lamprey (Petromyzon marinus) has provided insight into the origin and evolution of developmentalgenetic programs in vertebrates. We focus on recent work involving CRISPR/Cas9-mediated genome editing to study gene regulatory mechanisms involved in the development and evolution of neural crest cells and new cell types in the vertebrate nervous system, and transient transgenic assays that have been instrumental in dissecting the evolution of cis-regulatory control of gene expression in vertebrates. Finally, we discuss the broad potential for these functional genomic tools to address previously unanswerable questions related to the evolution of genomic regulatory mechanisms as well as issues related to invasive sea lamprey population control.

Development of the lamprey velum and implications for the evolution of the vertebrate jaw

“…The fossil record shows that most jawless groups became extinct during the Devonian period, in parallel with the acceleration of jawed vertebrate diversification 1,4 . Today, only one extant group of jawless vertebrates remains: the cyclostomes, comprised of lampreys and hagfishes 5,6 . The origin of jawed vertebrates during the Devonian period was a key event in early vertebrate history, as it enabled the transition from passive filter feeder to active predation.…”

“…1,4 Today, only one extant group of jawless vertebrates remains: the cyclostomes, comprised of lampreys and hagfishes. 5,6 The origin of jawed vertebrates during the Devonian period was a key event in early vertebrate history, as it enabled the transition from passive filter feeder to active predation. Although whether this shift was due to the Hiromasa Yokoyama, Miho Yoshimur, and Daichi G. Suzuki contributed equally to this work.…”

Evolutionary and Developmental Associations of Neural Crest and Placodes in the Vertebrate Head: Insights From Jawless Vertebrates

“…To do that requires that we compare developmental mechanisms between the two major lineages of vertebrates-the jawed and jawless clades-as well as a suitable outgroup, such as the invertebrate chordates. It is this simple but powerfully informative methodology that allows us to infer how developmental associations between neural crest and placodes evolved in the last common ancestor of vertebrates (Shimeld and Donoghue, 2012;York and McCauley, 2020a).…”

“…The extant jawless vertebrates, also known as the cyclostomes (Figure 3), are a monophyletic group of animals, and are the sole survivors of a diverse assemblage of jawless fishes that were among the first of their kind to evolve on this planet over 500 million years ago (Hardisty, 1979;Heimberg et al, 2010;Miyashita et al, 2019;York and McCauley, 2020a). They are represented by only two extant groups, the lampreys and hagfishes, which diverged from one another not too long after the cyclostome-gnathostome split.…”

“…This owes largely to the fact that lamprey adults and their embryos are relatively easy to obtain and rear in simple laboratory settings, at least compared to hagfish ( York et al, 2019a ; described below). Moreover, accessibility to annotated genomes and transcriptomes, as well as the application of modern molecular genetic techniques such as cell lineage tracing, overexpression of DNAs and RNAs, and knockdown/knockout experiments such as morpholinos and CRISPR/Cas9 genome editing has allowed researchers to address long-standing hypotheses concerning the origin and evolution of vertebrate traits, including neural crest and placodes ( McCauley and Bronner-Fraser, 2006 ; Smith et al, 2013 , 2018 ; Parker et al, 2014 ; Square et al, 2015 ; Zu et al, 2016 ; Hockman et al, 2019 ; York et al, 2019a ; York and McCauley, 2020a ).…”