Gill developmental program in the teleost mandibular arch
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Evaluation Summary:
In this manuscript, the authors use zebrafish histological staining, lineage tracing, enhancer transgenes, and mutants to find evidence for the gill origin of the vertebrate jaws hypothesis. This study nicely integrates into the literature on the origins of the mandibular jaw including discussion of fossil evidence and work in chondrichthyans and tests the hypotheses that the pseudobranch is derived from the mandibular arch, and that the pseudobranch is a segmental homolog of the gills. This paper will be impactful to the field of developmental biology both because the fate mapping methods used are generally applicable to a range of other lineage questions and because evidence for a gill arch origin of the jaw is an important contribution to vertebrate evolutionary biology.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Abstract
Whereas no known living vertebrate possesses gills derived from the jaw-forming mandibular arch, it has been proposed that the jaw arose through modifications of an ancestral mandibular gill. Here, we show that the zebrafish pseudobranch, which regulates blood pressure in the eye, develops from mandibular arch mesenchyme and first pouch epithelia and shares gene expression, enhancer utilization, and developmental gata3 dependence with the gills. Combined with work in chondrichthyans, our findings in a teleost fish point to the presence of a mandibular pseudobranch with serial homology to gills in the last common ancestor of jawed vertebrates, consistent with a gill origin of vertebrate jaws.
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Evaluation Summary:
In this manuscript, the authors use zebrafish histological staining, lineage tracing, enhancer transgenes, and mutants to find evidence for the gill origin of the vertebrate jaws hypothesis. This study nicely integrates into the literature on the origins of the mandibular jaw including discussion of fossil evidence and work in chondrichthyans and tests the hypotheses that the pseudobranch is derived from the mandibular arch, and that the pseudobranch is a segmental homolog of the gills. This paper will be impactful to the field of developmental biology both because the fate mapping methods used are generally applicable to a range of other lineage questions and because evidence for a gill arch origin of the jaw is an important contribution to vertebrate evolutionary biology.
(This preprint has been reviewed by eLife. …
Evaluation Summary:
In this manuscript, the authors use zebrafish histological staining, lineage tracing, enhancer transgenes, and mutants to find evidence for the gill origin of the vertebrate jaws hypothesis. This study nicely integrates into the literature on the origins of the mandibular jaw including discussion of fossil evidence and work in chondrichthyans and tests the hypotheses that the pseudobranch is derived from the mandibular arch, and that the pseudobranch is a segmental homolog of the gills. This paper will be impactful to the field of developmental biology both because the fate mapping methods used are generally applicable to a range of other lineage questions and because evidence for a gill arch origin of the jaw is an important contribution to vertebrate evolutionary biology.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
In this manuscript from the Crump laboratory, the authors use zebrafish histological staining, lineage tracing, enhancer transgenes, and mutants to find evidence for the gill origin of vertebrate jaws hypothesis. The data are mostly strong and convincing. I have only a few comments on some of the data and some suggestions for strengthening the discussion.
• This study nicely integrates into the literature on the origins of the mandibular jaw including discussion of fossil evidence and work in chondrichthyans. However, there is no discussion of jawless fish and how the considerable literature from species such as lamprey relates to the findings presented here. Do agnathans develop a pseudobranch?
• Are there gill-like structures derived from the second arch in teleosts? The authors mention the hemibranch …
Reviewer #1 (Public Review):
In this manuscript from the Crump laboratory, the authors use zebrafish histological staining, lineage tracing, enhancer transgenes, and mutants to find evidence for the gill origin of vertebrate jaws hypothesis. The data are mostly strong and convincing. I have only a few comments on some of the data and some suggestions for strengthening the discussion.
• This study nicely integrates into the literature on the origins of the mandibular jaw including discussion of fossil evidence and work in chondrichthyans. However, there is no discussion of jawless fish and how the considerable literature from species such as lamprey relates to the findings presented here. Do agnathans develop a pseudobranch?
• Are there gill-like structures derived from the second arch in teleosts? The authors mention the hemibranch derived from the hyoid arch in cartilaginous fishes. Is there a similar structure in any teleost? If there are no arch 2 gill-like structures, how this fits into the gill origin of jaw hypothesis should be discussed.
• The first sentence of the discussion is not fully supported by the data. More species need to be included to make this claim. This statement would need to be tempered.
• I like that the authors mention the alternative hypothesis in their discussion that "the pseudobranch arose independently from the jaw by co-option of a gill filament developmental program".
• More care needs to be taken with the word homology and to make the distinction between serial homology vs historical or functional homology. This manuscript would be stronger if it were to include a definition of these terms (or at least serial homology because that's the argument here). To avoid confusion, the authors should also specifically state serial homology when that's what the authors mean, for example in the second sentence of the discussion.
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Reviewer #2 (Public Review):
Thiruppathy and colleagues investigate pseudobranch development in a teleost fish, the zebrafish. The pseudobranch has long been hypothesized to be a vestigial mandibular arch gill. The classic model of jaw evolution in vertebrates posits that the gnathostome jaw evolved from modifications of an anterior gill-bearing segment. Here the authors were trying to test the hypotheses that (1) the pseudobranch is derived from the mandibular arch, and (2) that the pseudobranch is a segmental homolog of the gills.
One major strength of the methods and results is that they strongly support both hypotheses. The authors use cutting-edge fate mapping methods involving photoconversion of transgene-driven fluorophores as well as Cre-mediated lineage tracing to fate map mandibular arch mesenchyme and epithelium. By fate …
Reviewer #2 (Public Review):
Thiruppathy and colleagues investigate pseudobranch development in a teleost fish, the zebrafish. The pseudobranch has long been hypothesized to be a vestigial mandibular arch gill. The classic model of jaw evolution in vertebrates posits that the gnathostome jaw evolved from modifications of an anterior gill-bearing segment. Here the authors were trying to test the hypotheses that (1) the pseudobranch is derived from the mandibular arch, and (2) that the pseudobranch is a segmental homolog of the gills.
One major strength of the methods and results is that they strongly support both hypotheses. The authors use cutting-edge fate mapping methods involving photoconversion of transgene-driven fluorophores as well as Cre-mediated lineage tracing to fate map mandibular arch mesenchyme and epithelium. By fate mapping both neural crest-derived mesenchyme (by photoconverting sox10: kikGR, as well as labeling crest with a sox10:Cre excision of a stop cassette) and pharyngeal endoderm (by photoconverting fgf10b:nEOS) in the mandibular segment, the authors test for mandibular origins of two different pseudobranch progenitors (mesenchyme and epithelium). Another strength is including the enhancer activity of three different enhancers as a character to assess the serial homology of the pseudobranch and gills. A third strength is using gene function to test for serial homology by assessing pseudobranch and gill development in gata3 mutants.
One weakness is that the resolution of the photoconverted kikGR cells within the pseudobranch is low and visualizing individual cells is difficult in Figure 1e. However, the resolution of labeled crest cells in Fig. S1A is higher, and convincingly shows labeled neural crest cells in the center of the forming pseudobranch. A second weakness is that the fgf10b:nEOS expression, although strongest in the endodermal pouches, appears to also be more lowly expressed in non-endodermal cells.
Overall, the authors have achieved their goals and their conclusions of a first arch origin of the pseudobranch and likely serial homology between the pseudobranch and gills are both well supported.
The likely impact of this work, together with the cited 2022 bioRxiv paper (in which Hirschberger and Gillis show convincingly that the pseudobranch in a chondrichthyan is derived in part from mandibular arch pharyngeal endoderm and expresses similar gene expression patterns as gills during development) is high. Together the papers argue strongly that the pseudobranch is a mandibular arch-derived segmental homolog of a gill. These are exactly the kinds of data needed from extant gnathostomes to critically test the classic theory of a gill arch origin of the gnathostome jaw. As chondrichthyans are derived relative to the gnathostome stem ancestor, one possibility could be that the condition in chondrichthyans is derived and does not reflect the state of the gnathostome ancestor. This paper, in adding teleosts, argues against that scenario, as the more parsimonious explanation is that derived teleosts and chondrichthyans inherited a mandibular arch serial homolog of a gill from their common ancestor. This paper will likely have an impact on the field of developmental biology in that the fate mapping methods used are generally applicable to a range of other lineage questions. But the likely biggest impact will be on the field of vertebrate evolutionary biology, as together these two papers will be landmark studies arguing for a gill arch origin of the jaw, and strong motivations for paleontologists to look harder for fossils that can be evaluated for having a gill in the mandibular segment.
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