Adaptive responses to cool climate promotes persistence of a non-native lizard

Abstract

Successful establishment and range expansion of non-native species often require rapid accommodation of novel environments. Here, we use commongarden experiments to demonstrate parallel adaptive evolutionary response to a cool climate in populations of wall lizards (Podarcis muralis) introduced from southern Europe into England. Low soil temperatures in the introduced range delay hatching, which generates directional selection for a shorter incubation period. Non-native lizards from two separate lineages have responded to this selection by retaining their embryos for longer before ovipositionhence reducing the time needed to complete embryogenesis in the nest-and by an increased developmental rate at low temperatures. This divergence mirrors local adaptation across latitudes and altitudes within widely distributed species and suggests that evolutionary responses to climate can be very rapid. When extrapolated to soil temperatures encountered in nests within the introduced range, embryo retention and faster developmental rate result in one to several weeks earlier emergence compared with the ancestral state. We show that this difference translates into substantial survival benefits for offspring. This should promote short-and long-term persistence of nonnative populations, and ultimately enable expansion into areas that would be unattainable with incubation duration representative of the native range.

Developmental plasticity in reptiles: Insights from temperature‐dependent gene expression in wall lizard embryos

“…In April 2015, we collected 13 gravid females from Western France (around Pouzagues [46.788 N, –0.837 E] altitude: 258 m; will be referred to as Fr1), 15 from the French Pyrenees ([42.860 N, 1.105 E]; altitude: 1396 m; Fr2), 18 from lowland Tuscany (Greve in Chianti [43.588 N, 11.318 E], Colle di Val d'Elsa [43.428 N, 11.118 E], Certaldo [43.548 N, 11.042 E]; altitude: 83–245 m; It1), and 15 from the Tuscan Apennines (around Saltino [43.727 N, 11.538 E]; altitude: 966 m; It2). Although these populations experience different climatic conditions, partly as a result of differences in latitude and altitude, we did not necessarily expect any of them to be adapted to very low temperature, in contrast to the previously studied non‐native populations in England (Feiner, Rago, While, & Uller, ; While et al., ).…”

“…However, following oviposition in spring, soil temperatures can be substantially lower and embryos may need to maintain biological function and develop at temperatures well below 20°C. For example, thermal profiles of nests in non‐native populations in England frequently average below 20°C, with only brief periods of time at the higher temperatures typically used to incubate eggs in captivity (While et al., ). Similar climatic conditions occur at high altitude or latitude in their native range and, even within the warmer parts of the species’ distribution, soil temperatures could stay well below 20°C for days on end.…”

Patterns of developmental plasticity in response to incubation temperature in reptiles

“…It will therefore be important to carefully select traits for which fitness is unlikely to be thermally dependent or to understand the adaptive significance of plasticity. Empirical studies to date suggest that the extent of thermal developmental plasticity is quite variable between populations and species living in different climates, and at least sometimes this appears consistent with how climate should influence natural selection (e.g., Uller et al., ; While et al., ).…”

Extreme plasticity in reproductive biology of an oviparous lizard

“…More plausibly, selection over the almost 20 years (approximately four generations) of island life may have favored a shift toward prolonged uterine retention of eggs and thus an abbreviated subsequent incubation. This latter process has been documented in lacertid lizards ( Podarcis muralis ) translocated to cooler climates (Italy and France to the UK), over a similar time frame (20–80 years; While et al., 2015a). However, the within‐population variance in incubation periods was lower in that study (minimum incubation duration >87% of mean incubation period, across all populations at both temperatures tested: While et al., 2015b) than in the Swedish sand lizards (minimum incubation duration 55% of mean incubation period for the island lizards, 71% for Asketunnan lizards).…”