Strong impact of thermal environment on the quantitative genetic basis of a key stress tolerance trait

TY - JOUR

T1 - Strong impact of thermal environment on the quantitative genetic basis of a key stress tolerance trait

AU - Ørsted, Michael

AU - Hoffmann, Ary Anthony

AU - Rohde, Palle Duun

AU - Sørensen, Peter

AU - Kristensen, Torsten Nygård

PY - 2019/3

Y1 - 2019/3

N2 - Most organisms experience variable and sometimes suboptimal environments in their lifetime. While stressful environmental conditions are normally viewed as a strong selective force, they can also impact directly on the genetic basis of traits such as through environment-dependent gene action. Here, we used the Drosophila melanogaster Genetic Reference Panel to investigate the impact of developmental temperature on variance components and evolutionary potential of cold tolerance. We reared 166 lines at five temperatures and assessed cold tolerance of adult male flies from each line and environment. We show (1) that the expression of genetic variation for cold tolerance is highly dependent on developmental temperature, (2) that the genetic correlation of cold tolerance between environments decreases as developmental temperatures become more distinct, (3) that the correlation between cold tolerance at individual developmental temperatures and plasticity for cold tolerance differs across developmental temperatures, and even switches sign across the thermal developmental gradient, and (4) that evolvability decrease with increasing developmental temperatures. Our results show that the quantitative genetic basis of low temperature tolerance is environment specific. This conclusion is important for the understanding of evolution in variable thermal environments and for designing experiments aimed at pinpointing candidate genes and performing functional analyses of thermal resistance.

AB - Most organisms experience variable and sometimes suboptimal environments in their lifetime. While stressful environmental conditions are normally viewed as a strong selective force, they can also impact directly on the genetic basis of traits such as through environment-dependent gene action. Here, we used the Drosophila melanogaster Genetic Reference Panel to investigate the impact of developmental temperature on variance components and evolutionary potential of cold tolerance. We reared 166 lines at five temperatures and assessed cold tolerance of adult male flies from each line and environment. We show (1) that the expression of genetic variation for cold tolerance is highly dependent on developmental temperature, (2) that the genetic correlation of cold tolerance between environments decreases as developmental temperatures become more distinct, (3) that the correlation between cold tolerance at individual developmental temperatures and plasticity for cold tolerance differs across developmental temperatures, and even switches sign across the thermal developmental gradient, and (4) that evolvability decrease with increasing developmental temperatures. Our results show that the quantitative genetic basis of low temperature tolerance is environment specific. This conclusion is important for the understanding of evolution in variable thermal environments and for designing experiments aimed at pinpointing candidate genes and performing functional analyses of thermal resistance.

KW - ADAPTATION

KW - ARCHITECTURE

KW - COLD TOLERANCE

KW - DEVELOPMENTAL TEMPERATURE

KW - DROSOPHILA-MELANOGASTER

KW - EVOLUTION

KW - HEAT TOLERANCE

KW - PHENOTYPIC PLASTICITY

KW - RESISTANCE

KW - SELECTION

U2 - 10.1038/s41437-018-0117-7

DO - 10.1038/s41437-018-0117-7

M3 - Journal article

C2 - 30050062

SN - 0018-067X

VL - 122

SP - 315

EP - 325

JO - Heredity

JF - Heredity

IS - 3

ER -