Convergent gene family evolution underpins repeated transitions to metamorphic development across Pancrustacea

Abstract

Arthropod developmental modes are highly diverse, ranging from direct development with little morphological change between moults to metamorphic life-stage progressions characterised by profound transformations. Metamorphosis can be defined as a post-embryonic life-stage progression event leading to adulthood that is characterised by major morphological changes and modifications of the adaptive landscape. Within this framework, we compare four independent evolutionary life history transitions to metamorphic development across Pancrustacea. Using a phylogenomic dataset of 54 species spanning 26 orders, we investigated gene family evolutionary dynamics associated with the inferred origins of metamorphosis in Insecta, Copepoda, Eucarida, and Thecostraca. Compared with non-metamorphic sister lineages as well as descendent and ancestral nodes, transitions to metamorphic development were consistently associated with elevated gene family births and expansions. Although these expansions predominantly involved different gene families in each lineage, they repeatedly converged on shared biological functions, particularly those related to embryonic and post-embryonic development, morphogenesis, nervous system differentiation, and other processes relevant to the biology and evolution of metamorphosis. Evolutionary modelling further identified a subset of gene families exhibiting adaptive, lineage-specific expansions, including genes implicated in neural and sensory development, segmentation, and moulting. Together, these findings support a model in which independent transitions to metamorphic development repeatedly recruited different components of a shared developmental toolkit, achieving functional convergence through distinct genetic trajectories. This reframes the arthropod moulting programme as an evolutionarily flexible developmental substrate whose repeated modification has facilitated the emergence of complex multi-phasic life histories and contributed to the extraordinary diversification of Pancrustacea.