Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia

Abstract

Drosophila melanogaster invaded Australia around 100 years ago, most likely through a northern invasion. The wide range of climatic conditions in eastern Australia across which D. melanogaster is now found provides an opportunity for researchers to identify traits and genes that are associated with climatic adaptation. Allozyme studies indicate clinal patterns for at least four loci including a strong linear cline in Adh and a non-linear cline in alpha-Gpdh. Inversion clines were initially established from cytological studies but have now been validated with larger sample sizes using molecular markers for breakpoints. Recent collections indicate that some genetic markers (Adh and In(3R)Payne) have changed over the last 20 years reflecting continuing evolution. Heritable clines have been established for quantitative traits including wing length/area, thorax length and cold and heat resistance. A cline in egg size independent of body size and a weak cline in competitive ability have also been established. Postulated clinal patterns for resistance to desiccation and starvation have not been supported by extensive sampling. Experiments under laboratory and semi-natural conditions have suggested selective factors generating clinal patterns, particularly for reproductive patterns over winter. Attempts are being made to link clinal variation in traits to specific genes using QTL analysis and the candidate locus approach, and to identify the genetic architecture of trait variation along the cline. This is proving difficult because of inversion polymorphisms that generate disequilibrium among genes. Substantial gaps still remain in linking clines to field selection and understanding the genetic and physiological basis of the adaptive shifts. However D. melanogaster populations in eastern Australia remain an excellent resource for understanding past and future evolutionary responses to climate change.

Impacts of climate warming on terrestrial ectotherms across latitude

“…The capacity of ectotherms to acclimate their physiological performance curves is generally low in tropical species (10,11,16,24). Adaptive evolutionary responses should also ameliorate the impacts of warming, but we currently lack a strong empirical or theoretical foundation upon which to assess the potential for evolutionary responses among tropical ectotherms to the rapid rates of projected warming (32,33). Changes in behavior, including shifts in the timing of activity, and changes in range boundaries have been documented particularly at high latitudes (3,4,34,35), but such phenological shifts may be caused by either enhanced or reduced fitness.…”

Genomic Differentiation Between Temperate and Tropical Australian Populations ofDrosophila melanogaster

“…The majority of work on these clines has investigated various phenotypic traits, chromosome inversion polymorphisms, and enzyme-coding genes (Sezgin et al 2004), as well as several other genes harboring clinal variants (Costa et al 1992;McColl and McKechnie 1999;Schmidt et al 2000;Duvernell et al 2003). The cline along the east coast of Australia has received considerable recent attention due to the efforts of Ary Hoffmann and collaborators (e.g., Hoffmann and Weeks 2007). The fact that similar clines are often observed on different continents strongly implicates natural selection rather than demography as the cause of clinal variation (Oakeshott et al , 1983Singh and Rhomberg 1987;Singh 1989;Singh and Long 1992;Gockel et al 2001;Kennington et al 2003;Hoffmann and Weeks 2007).…”

“…The cline along the east coast of Australia has received considerable recent attention due to the efforts of Ary Hoffmann and collaborators (e.g., Hoffmann and Weeks 2007). The fact that similar clines are often observed on different continents strongly implicates natural selection rather than demography as the cause of clinal variation (Oakeshott et al , 1983Singh and Rhomberg 1987;Singh 1989;Singh and Long 1992;Gockel et al 2001;Kennington et al 2003;Hoffmann and Weeks 2007). Importantly, although cosmopolitan chromosome inversion polymorphisms exhibit latitudinal clines (with inversion frequency increasing in more tropical populations), many observations convincingly show that inversions explain only a fraction of clinal variation, even for genes located in inverted regions (Voelker et al 1978;Knibb 1982;Singh and Rhomberg 1987;Frydenberg et al 2003;Umina et al 2006).…”

Long-Term and Short-Term Evolutionary Impacts of Transposable Elements onDrosophila

“…Within North America, where there is the largest set of pre-P-element strains, spatial locations are disperse: strains were collected on the West and the East Coast as well as in the northern and southern latitudes. Latitudinal clines for various loci have been observed in D. melanogaster (reviewed in Schmidt et al 2005;Hoffmann and Weeks 2007). Unfortunately, this may increase the possibility of falsely concluding that there is temporal genetic differentiation while the actual difference would be a result of the geographic heterogeneity of between-time samples.…”