Developmental Basis and Consequences of a Key Innovation in Lungless Salamanders

Abstract

A longstanding goal of evolutionary developmental biology is to document the precise mechanisms that underlie formation of, and differences among, basic body plans, organ systems and physiological functions. Another, less‐studied approach is to reveal how those mechanisms are perturbed to enable, or even mediate, the origin of novel adaptations that are critical for the evolutionary success of individual clades. I will report results of our recent studies of evolutionary lung loss in plethodontid salamanders and of the correlated evolution of cutaneous respiration, which is the principal mode of respiratory gas exchange in all 478 species in this, the largest family of extant urodeles. Surprisingly, plethodontids are not entirely lungless: a lung rudiment forms initially in embryos but is resorbed before hatching. Some embryonic cells express lung‐associated molecular markers, such as the gene Nkx2.1, although at lower levels than in lunged species. Moreover, elevated levels of TGF‐ß signaling, which is known to mediate Nkx2.1 expression during normal lung development, may be part of the genetic mechanism responsible for lung loss. In contrast, we have discovered in salamanders a novel paralog of the gene surfactant‐associated protein C (SFTPC), which is a critical component of pulmonary surfactant expressed exclusively in the lung in other vertebrates. In plethodontids, however, and only in plethodontids, this gene is expressed in novel sites of respiration outside the lungs and at different sites in larvae vs. adults that correlate with gas exchange. These and other changes to the ancestral urodele ontogeny may have contributed to the remarkable evolutionary radiation of the lungless salamanders.