Many factors contribute to colonization success in novel habitats. Anoles, as a group, are particularly adept at establishing in new areas. Urban ecosystems are no exception. A diversity of studies have sought to understand how adult anoles conquer human-modified habitats, but relatively little attention has been given to earlier life-stages (e.g., eggs). The brown anole (Anolis sagrei) and the crested anole (Anolis cristatellus) (Figure 1) are two species that have received considerable attention. Although these two species are quite similar in morphology and habitat preference (i.e. both trunk-ground anoles), work from Jason Kolbe’s lab (e.g. Battles and Kolbe 2019), shows that adults differ in thermal preference: A. sagrei prefers warmer, open-canopy habitats while A. cristatellus prefers cooler, closed-canopy habitats. Because temperatures are unusually high in urban areas (i.e. the urban heat island), the spread of A. cristatellus may be limited throughout the urban matrix compared to A. sagrei.
But what about eggs? Two recent studies suggest that A. sagrei nests reach warmer temperatures than those of A. cristatellus (Sanger et al., 2018, Tiatragul et al., 2019), thus, like adults, A. sagrei embryos may be more robust to high temperatures. Is it possible that thermal tolerance of embryos differ between these two species? If so, this may also help explain why A. sagrei has been much more successful at colonizing urban habitats where ground (and nest) temperatures are usually much warmer than in adjacent rural or natural areas (Tiatragul et al., 2017).
In a study recently published in the Journal of Experimental Biology (Hall and Warner 2019), we subjected eggs of A. sagrei and A. cristatellus to extreme fluctuations in temperature modeled from nests in urban environments. We found that A. sagrei embryos have a thermal tolerance approximately 2 degrees Celsius higher than A. cristatellus. This indicates that the thermal physiology of embryos is adapted to species-specific nest temperatures (though we discuss other possible explanations as well). Regardless, thermal tolerance differs widely between these two species, and this may help explain species-specific patterns of occupancy throughout the urban matrix.
As a side note (that I reluctantly removed from the manuscript during the review process – long sigh), although the Anolis radiation, which includes nearly 400 species, is considered a model system for studying adaptive radiation, to our knowledge, studies never consider that embryo phenotypes and egg survival may be an important driver of speciation. This is particularly important for two reasons. First, egg survival is a vital determinant of population cycles for these lizards (Andrews 1988), and likely plays a vital role in population viability, survival, and colonization success (Losos et al., 2003). Second, this adaptive radiation is characterized by many dispersal events, often from and to small islands throughout the Caribbean (Poe et al., 2018). Although key innovations, phenotypic plasticity, niche expansion and other processes are considered important in such dispersals, these processes are always evaluated from the perspective of adult phenotypes. Successful embryo development, however, is a requirement for persistence in every environment. Given that general protocols exist for embryo collection and analysis (Sanger et al., 2008a,b), we suggest this system is ripe for a relatively broad phylogenetic analysis of embryo physiology. Such work would illuminate the importance of embryo adaptation in colonizing novel environments (e.g. urban landscapes) and responding to environmental perturbances (e.g. climate change), and give us something to talk about other than dewlaps and limb lengths (which would make me happy).
Andrews, R.M., 1988. Demographic correlates of variable egg survival for a tropical lizard. Oecologia, 76(3), pp.376-382.
Battles, A.C. and Kolbe, J.J., 2019. Miami heat: Urban heat islands influence the thermal suitability of habitats for ectotherms. Global Change Biology, 25(2), pp.562-576.
Hall, J.M. and Warner, D.A., 2019. Thermal tolerance in the urban heat island: thermal sensitivity varies ontogenetically and differs between embryos of two sympatric ectotherms. Journal of Experimental Biology, 222(19), p.jeb210708.
Losos, J.B., Schoener, T.W. and Spiller, D.A., 2003. Effect of immersion in seawater on egg survival in the lizard Anolis sagrei. Oecologia, 137(3), pp.360-362.
Poe, S., de Oca, A.N.M., Torres-Carvajal, O., de Queiroz, K., Velasco, J.A., Truett, B., Gray, L.N., Ryan, M.J., Köhler, G., Ayala-Varela, F. and Latella, I., 2018. Comparative evolution of an archetypal adaptive radiation: innovation and opportunity in Anolis lizards. The American Naturalist, 191(6), pp.E185-E194.
Sanger, T.J., Hime, P.M., Johnson, M.A., Diani, J. and Losos, J.B., 2008a. Laboratory protocols for husbandry and embryo collection of Anolis lizards. Herpetological Review, 39(1), pp.58-63.
Sanger, T.J., Losos, J.B. and Gibson‐Brown, J.J., 2008b. A developmental staging series for the lizard genus Anolis: a new system for the integration of evolution, development, and ecology. Journal of Morphology, 269(2), pp.129-137.
Sanger, T.J., Kyrkos, J., Lachance, D.J., Czesny, B. and Stroud, J.T., 2018. The effects of thermal stress on the early development of the lizard Anolis sagrei. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 329(4-5), pp.244-251.
Tiatragul, S., Kurniawan, A., Kolbe, J.J. and Warner, D.A., 2017. Embryos of non-native anoles are robust to urban thermal environments. Journal of Thermal Biology, 65, pp.119-124.
Tiatragul, S., Hall, J.M., Pavlik, N.G. and Warner, D.A., 2019. Lizard nest environments differ between suburban and forest habitats. Biological Journal of the Linnean Society, 126(3), pp.392-403.
