Progeny ofXenopus laevisfrom altitudinal extremes display adaptive physiological performance

Abstract

Environmental temperature variation generates adaptive phenotypic differentiation in widespread populations. We used a common garden experiment to determine whether offspring with varying parental origins display adaptive phenotypic variation related to different thermal conditions experienced in parental environments. We compared burst swimming performance and critical thermal limits of African clawed frog (Xenopus laevis) tadpoles bred from adults captured at high (∼ 2000 m above sea level) and low (∼ 5 m above sea level) altitudes. Maternal origin significantly affected swimming performance. Optimal swimming performance temperature had a >9°C difference between tadpoles with low altitude maternal origins (Topt: pure- and cross-bred 35.0°C) and high altitude maternal origins (Topt: pure-bred 25.5°C, cross-bred 25.9°C). Parental origin significantly affected critical thermal limits. Pure-bred tadpoles with low altitude parental origins had higher CTmax (37.8±0.8°C) than pure-bred tadpoles with high altitude parental origins and all cross-bred tadpoles (37.0±0.8 and 37.1±0.8°C). Pure-bred tadpoles with low altitude parental origins and all cross-bred tadpoles had higher CTmin (4.2±0.7 and 4.2±0.7°C) than pure-bred tadpoles with high altitude parental origins (2.5±0.6°C). Our study shows Xenopus laevis tadpoles’ varying thermal physiological traits is the result of adaptive responses to their parental thermal environments. This study is one of few demonstrating potential intraspecific evolution of critical thermal limits in a vertebrate species. Multi-generation common garden experiments and genetic analyses would be required to further tease apart the relative contribution of plastic and genetic effects to the adaptive phenotypic variation observed in these tadpoles.

Growing up in a new world: trait divergence between rural, urban, and invasive populations of an amphibian urban invader

“…All tadpoles that underwent morphological measurements were also tested for swimming performance on the same day. Performance trials were carried out in a clear plexiglass tank (30 × 5 cm) filled with 3 cm of aged tap water (Wagener et al 2021).…”

Population genomics ofXenopus laevisin southern Africa

“…New samples analyzed here from Sentinel Peak in Letseng, a high altitude area in the Drakensburg portion of the Great Escarpment, which is >3,000 m above sea level (asl), were not substantially differentiated from a population near Kimberly, which is ∼1,100 m asl. This suggests that genome-wide genetic changes associated with adaptation to high altitude (see Wagener et al 2021) are small in comparison to population structure within X. laevis .…”

“…Phenotypic variation exists within X. laevis , such as size differences (larger in the SW) and variation in gonadal morphology, with a higher frequency of testicular ovarian follicles detected in animals originating from northeast compared to southwest South Africa (Du Preez et al 2009). Reciprocal translocation experiments suggest adaptation to different rainfall and altitudinal regimes, as well as variation in the extent of plasticity of tadpoles to adjust to these regimes (Wagener et al 2021; Kruger et al 2022). Overall, the substantial and complex population structure of X. laevis coupled with its wide use as an experimental organisms and new role as an invasive species, underscores the importance of understanding genetic variation in natural populations and how this relates to diversity in captive and invasive populations.…”

More time for aliens? Performance shifts lead to increased activity time budgets propelling invasion success

“…For adult frogs, Araspin et al (2020) measured endurance distance (EndDist), which is relevant in the context of mate-searching or dispersal and they found rapid shifts in the temperature dependence of locomotor performance. For tadpoles, maximum velocity (MaxVel) was recorded by Kruger (2020) and Wagener et al (2021), which is relevant in the context of predator escape. They used common garden experiments to determine whether tadpoles with varying parental origins show adaptive phenotypic variation related to different temperatures experienced in parental environments.…”

“…They used common garden experiments to determine whether tadpoles with varying parental origins show adaptive phenotypic variation related to different temperatures experienced in parental environments. For thermal performance trials and breeding of adults, we used specimens collected in the native region from KwaZulu-Natal (summer rainfall region, data from Wagener et al 2021) and Stellenbosch (Western Cape province, winter rainfall region, Kruger 2020), South Africa and the French invasive area from the Département Deux-Sèvres, France (data from Kruger 2020; Araspin et al 2020). For climatic information of the three regions see Supplementary Material S1.…”