Evidence for the evolution of thermal tolerance, but not desiccation tolerance, in response to hotter, drier city conditions in a cosmopolitan, terrestrial isopod

Abstract

Cities are often hotter and drier compared with nearby undeveloped areas, but how organisms respond to these multifarious stressors associated with urban heat islands is largely unknown. Terrestrial isopods are especially susceptible to temperature and aridity stress as they have retained highly permeable gills from their aquatic ancestors. We performed a two temperature common garden experiment with urban and rural populations of the terrestrial isopod, Oniscus asellus, to uncover evidence for plastic and evolutionary responses to urban heat islands. We focused on physiological tolerance traits including tolerance of heat, cold, and desiccation. We also examined body size responses to urban heat islands, as size can modulate physiological tolerances. We found that different mechanisms underlie responses to urban heat islands. While evidence suggests urban isopods may have evolved higher heat tolerance, urban and rural isopods had statistically indistinguishable cold and desiccation tolerances. In both populations, plasticity to warmer rearing temperature diminished cold tolerance. Although field-collected urban and rural isopods were the same size, rearing temperature positively affected body size. Finally, larger size improved desiccation tolerance, which itself was influenced by rearing temperature. Our study demonstrates how multifarious changes associated with urban heat islands will not necessarily contribute to contemporary evolution in each of the corresponding physiological traits.

Keywords: adaptation; body size; global change; plasticity; urban evolution.

FIGURE 1

(a) Diurnal plot of temperature (°C) values (mean temperature ± 1 SD for each hour of the day) among urban and rural collection sites shown as orange and blue, respectively. (b) Diurnal plot of relative humidity (%) values (mean RH ± 1 SD for each hour of the day) among urban and rural sites shown as orange and blue, respectively. Temperature and relative humidity were recorded at thirty‐minute intervals from August to October in isopod refugia. (c) Impervious surface area map of Cleveland, Ohio, USA (data from Elvidge et al., 2007). High ISA values are shown as warm colors and low ISA values are shown as cool colors, with blue designating 0%–10% ISA and red designating 90%–100% ISA. Rural collection sites are represented by white circles, and urban collection sites are represented by white triangles

FIGURE 2

Results for: (a) body mass (mg) as a function of source habitat for field‐caught isopods, and (b) body mass (mg) as a function of temperature treatment across urban and rural populations for laboratory‐reared isopods. Predicted values ± 1 SE from linear mixed effects models are shown, with the urban population in triangle symbols and the rural population in circles

FIGURE 3

Thermal tolerance responses across urban and rural populations reared under two temperature treatments. Results for: (a) CT_max (critical thermal maximum, °C), (b) CT_min (critical thermal minimum, °C), and (c) thermal tolerance breadth (CT_max–CT_min, °C) as functions of rearing temperature (21 and 29°C). Predicted values ±1 SE from linear mixed effects models are shown, with the urban population in triangle symbols and the rural population in circles

FIGURE 4

Structural equation model of how body mass, rearing temperature, and source population affect desiccation tolerance. Solid lines indicate positive paths and dashed lines indicate negative paths. Line width is proportional to the standardized path coefficient shown above each line. Asterisks indicate significant paths at the 0.05 level