Male sterility at extreme temperatures: a significant but neglected phenomenon for understanding Drosophila climatic adaptations

Abstract

The thermal range for viability is quite variable among Drosophila species and it has long been known that these variations are correlated with geographic distribution: temperate species are on average more cold tolerant but more heat sensitive than tropical species. At both ends of their viability range, sterile males have been observed in all species investigated so far. This symmetrical phenomenon restricts the temperature limits within which permanent cultures can be kept in the laboratory. Thermal heat sterility thresholds are very variable across species from 23 degrees C in heat sensitive species up to 31 degrees C in heat tolerant species. In Drosophila melanogaster, genetic variations are observed among geographic populations. Tropical populations are more tolerant to heat induced sterility and recover more rapidly than temperate ones. A genetic analysis revealed that about 50% of the difference observed between natural populations was due to the Y chromosome. Natural populations have not reached a selection limit, however: thermal tolerance was still increased by keeping strains at a high temperature, close to the sterility threshold. On the low temperature side, a symmetrical reverse phenomenon seems to exist: temperate populations are more tolerant to cold than tropical ones. Compared to Mammals, drosophilids exhibit two major differences: first, male sterility occurs not only at high temperature, but also at a low temperature; second, sterility thresholds are not evolutionarily constrained, but highly variable. Altogether, significant and sometimes major genetic variations have been observed between species, between geographic races of the same species, and even between strains kept in the laboratory under different thermal regimes. In each case, it is easily argued that the observed variations correspond to adaptations to climatic conditions, and that male sterility is a significant component of fitness and a target of natural selection.

Phenology of spotted wing drosophila in the San Joaquin Valley varies by season, crop and nearby vegetation

“…Other studies have shown similar declines in trap captures as well as reductions in survival and fecundity at high temperatures (David et al 2005;Kinjo et al 2014;Tochen et al 2014). The negative effects of high summer temperatures on SWD may explain why SWD has not become a pest of commercial stone fruit and grapes, which are primarily harvested from July to October in the San Joaquin Valley.…”

YNot a Dead End: Epistatic Interactions BetweenY-Linked Regulatory Polymorphisms and Genetic Background Affect Global Gene Expression inDrosophila melanogaster

“…Therefore we suggest that our findings of Drosophila immune response genes being responsive to YRV are most likely explained by variation in noncoding components of the Y chromosome, such as repeat copy number. D. melanogaster populations from France and India are known to differ in the thermal sensitivity of spermatogenesis (Rohmer et al 2004;David et al 2005), with temperate and tropical Y chromosomes contributing substantially to this difference. Among genes that show YRV in at least two of the three backgrounds, we find candidates known to be structural constituents of cytoskeleton (nod, CG9279, and tm2) and lipid metabolism (CG9914, CG17292, CG9458, CG11426, CG6295, CG6277, CG18815, and CG31872).…”

“…Spermatogenesis in Drosophila males is extremely sensitive to heat, with males becoming sterile anywhere from 23°in heatsensitive species to 31°in heat-tolerant species (Chakir et al 2002;David et al 2005). In D. melanogaster, Rohmer et al (2004) found that differences between Y chromosome lineages from tropical and temperate regions are responsible for much of the variation in thermal sensitivity of spermatogenesis.…”

Interspecific Y chromosome variation is sufficient to rescue hybrid male sterility and is influenced by the grandparental origin of the chromosomes

“…Instead, most if not all of the~14 protein-coding genes present on the Y chromosomes of Drosophila melanogaster, D. simulans and other closely related species have male-specific functions and are exclusively expressed in the testis (Gepner and Hays, 1993;Carvalho et al, 2000;Carvalho et al, 2001;Vibranovski et al, 2008). Nevertheless, a suite of studies have shown that genetic variation present on the Y of Drosophila underlie phenotypic variation in male fitness (Chippindale and Rice, 2001;Yee et al, 2015), sex ratio distortion (Carvalho et al, 1997;Montchamp-Moreau et al, 2001;Branco et al, 2013a, b), tolerance to temperature extremes (Rohmer et al, 2004;David et al, 2005), behavior (Stoltenberg and Hirsch, 1997;Huttunen and Aspi, 2003), gene expression (Lemos et al, 2008;Sackton et al, 2011;Branco et al, 2013a, b) and chromatin states in somatic tissues .…”