Compounding heterochrony shapes the salamander visual system across adaptive zones

Transitioning between disparate environments presents new physical challenges, and metamorphosis can provide solutions. The life cycles of most amphibians involve an aquatic-to-terrestrial transition and concomitant metamorphosis, but shifts in developmental timing (heterochrony) have also produced a wide variety of aquatic-only and terrestrial-only forms. Thyroid hormone (TH) signalling can govern the timing of tissue transformation and may be a key mechanism behind the relationship between development and diversification of some metamorphic traits. Here, we show that life cycle mode and cave adaptation (troglomorphy) through heterochrony primarily explain variation in salamander eyes and retina. Across levels of organization (organ/tissue), heterochrony led to serial reductions in the visual system of larval-form paedomorphs that lost metamorphosis. This pattern is compounded in larval-form paedomorphic lineages that subsequently transitioned to subterranean environments and evolved troglomorphic traits. Following Haller's Rule, visual system investment declines across ontogeny but at a faster rate in paedomorphs and even faster (for eye size) in troglomorphs. Thyroid hormone typically increases eye size during metamorphosis; however, we show that responsiveness is reduced in paedomorphs and lost or reversed in troglomorphs. Salamander visual system variation is an example of how alterations to hormone-mediated transformation can shift developmental trajectories and compound phenotypic modifications as species move into more divergent environments.