Discrete embryonic character variation uncovers hidden ecological adaptations in lacertid lizards.

Abstract

Embryogenesis is the first step in the ontogenetic life journey of any individual, and is thus a starting point for natural selection to cause evolutionary change. There are slight variations in the timing of embryonic development, known as heterochrony, which may eventually lead to major differences in adult anatomy. To test this hypothesis, the embryonic development of three closely related lizard species, Darevskia armeniaca, Lacerta agilis, and L. viridis, which are adapted to different habitats, was compared by analyzing discrete timing characters. Both intra- and interspecific variation was detected. The latter may be interpreted as embryonic pre-adaptions to later adult lifestyles, demonstrating that developmental penetrance manifests within a few million years. Traits with large intraspecific temporal variation, such as limb-related features, were susceptible to natural selection. In particular, the mountain-dwelling, climbing species D. armeniaca showed embryonic preadaptions by an early developing limb anlagen. This observation demonstrated interspecific variation, which was elusive in a previous comparative study based on purely metric data of developing limb lengths, and highlighted the importance of multiple data sources to draw robust conclusions about evolutionary change. Timing differences indicated unexplored ecological adaptations of the poorly understood lifestyle of these lizards. Thus, embryonic research provides a platform to explore superficially hidden evolutionary adaptations of all organisms on Earth.