In a new study published this week in the journal Science Advances, scientists used morphological, molecular, and experimental approaches to examine members of the Plethodontidae, a dominant family of salamanders, all of which are lungless as adults.
Plethodontidae is the largest family of salamanders, with over 400 species in four subfamilies. It accounts for more than two-thirds of extant salamander diversity.
Its members occur predominantly in the Americas from southern Canada to the Amazon basin in Brazil; a few species occur in Sardinia, northern Italy, and the Korean peninsula.
All adult plethondontids lack lungs, breathing entirely through nonpulmonary tissues, mainly the skin and the mucus membranes in the mouth and throat.
Lung loss has occurred independently at least four times among distantly related amphibians and there are other instances of lung reduction or loss in both amphibians and some vertebrates.
While the adaptive significance and ecological context of lung loss in plethodontids are highly debated, little is known about its developmental underpinnings
The discovery of lunglessness in plethodontids in the 19th century triggered the search for a vestigial lung.
The most extensive study was by Cornell University doctoral student Amy Grace Mekeel in the 1920s, who compared lung morphogenesis in the spotted salamander (Ambystoma maculatum) to development in plethodontids. Although Mekeel could find no trace of a lung in adult plethodontids, she described in her dissertation incipient stages of lung development in embryos: a lung rudiment is present transiently but disappears before hatching.
Unfortunately, except for a single conference abstract, Mekeel’s research was never published and her work is largely forgotten. Moreover, researchers have largely neglected this phenomenon over the subsequent 90 years.
“Clearly lungless salamanders do fine without lungs given that they make up about two-thirds of all salamander species; perhaps losing lungs enabled, rather than hindered, this remarkable evolutionary success,” said Dr. Zachary Lewis, a researcher in the Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology at Harvard University.
In the study, Dr. Lewis and colleagues employed histology and micro-CT to examine the morphology of lung development in both lung and lungless salamanders.
They found that lungless salamanders begin developing lungs as embryos in much the same way as species with lungs develop them.
They then used in situ hybridization and RNA-sequencing to show that the structure that forms during lungless salamander embryonic development resembles a lung not just morphologically, but also in terms of the molecules expressed.
They hypothesize that lung development ceases in these species due to a lack of cues that maintain lung development which arise from the tissue, mesenchyme, that surrounds the lung as it develops.
“We put mesenchyme from a salamander with lungs into a lungless salamander embryo and allowed it to develop. It resulted in the formation of structures that resemble lungs, offering some evidence that lungless salamanders remain capable of continuing to develop lungs,” Dr. Lewis said.
The team’s findings also confirm Amy Grace Mekeel’s doctoral thesis.
“The lung precursor appears and disappears before the lungless salamander embryos hatch, just as Mekeel described,” said Dr. Ryan Kerney, a researcher in the Department of Biology at Gettysburg College.
“This work vindicates Mekeel’s earlier thesis and lays the initial adult vestige hypothesis to rest.”
The study reveals that lung developmental-genetic pathways are at least partially conserved despite the absence of functional adult lungs for at least 25 and possibly exceeding 60 million years.
Understanding the evolution of lung loss in Plethondontidae could also shed light on organ loss in other vertebrates.
“In the future, if these genetic mechanisms are revealed, we will have a more complete understanding of how evolution acts to do away with an organ such as the lung, which was long thought critical to achieving life on land,” Dr. Lewis said.
Zachary R. Lewis et al. 2022. Developmental basis of evolutionary lung loss in plethodontid salamanders. Science Advances 8 (33); doi: 10.1126/sciadv.abo6108
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