Enhanced fertility and chill tolerance after cold-induced reproductive arrest in females of temperate species of the Drosophila buzzatii complex

Abstract

Long-term exposure to low temperatures during adult maturation might decrease fertility after cold recovery as a consequence of carryover effects on reproductive tissues. This pattern should be more pronounced in tropical than in temperate species as protective mechanisms against chilling injuries are expected to be more effective in the latter. We initially determined the lower thermal thresholds to induce ovarian maturation in four closely related Drosophila species, two inhabiting temperate regions and the other two tropical areas of South America. As expected, only temperate species regularly experience cold-inducing conditions for reproductive arrest during winter in their natural environment. Subsequently, we exposed reproductively arrested and mature females to cold-inducing conditions for reproductive arrest over a long period. Following cold exposure, tropical species exhibited a dramatic fertility decline, irrespective of reproductive status. In contrast, not only were temperate females fecund and fertile but also fertility was superior in females that underwent cold-induced reproductive arrest, suggesting that it might act as a protecting mechanism ensuring fertility after cold recovery. Based on these findings, we decided to evaluate the extent to which reproductive status affects cold tolerance and energy metabolism at low temperature. We found a lower metabolic rate and a higher cold tolerance in reproductively arrested females, although only temperate species attained high levels of chill tolerance. These findings highlight the role of cold-induced reproductive arrest as part of an integrated mechanism of cold adaptation that could potentially contribute to the spread of temperate species into higher latitudes or altitudes.

Cold acclimation triggers major transcriptional changes in Drosophila suzukii

“…Expression of chorion-related genes follows this pattern as highest expression has been reported at intermediate temperatures [49]. The lowest developmental thermal threshold for ovarian maturation is generally around 10–12 °C in temperate drosophilids [99]. In D. suzukii , studies reported a reproductive dormancy mainly due to development at low temperature [33, 34, 37].…”

“…It is not clear whether arrest of oogenesis is a passive consequence of low temperature with no adaptive value for cold tolerance or whether this mechanism is an active protective strategy. Data from drosophila species support that cold-induced oogenesis arrest (via quiescence or diapause) is actually part of an integrated mechanism of cold adaptation and cold stress tolerance mechanism [99, 101].…”

Thermal stress causes DNA damage and mortality in a tropical insect

“…It results that temperate populations are usually better able to cope with low temperature stress than their tropical counterparts, as reported in flesh flies for instance (Chen et al, 1990). Likewise, Drosophila species from tropical origins are often much less cold tolerant than species found in temperate areas (Gibert et al, 2001;Goto and Kimura, 1998;Kellermann et al, 2012;Mensch et al, 2017;Olsson et al, 2016). However, whether species adapted to tropical climates are capable of tolerating cold stress, and by which physiological mechanisms they can do so, remains a poorly explored question.…”

Divergent metabolomic profiles of cold-exposed mature and immature females of tropical versus temperate Drosophila species

“…Figure S1 shows the phylogenetic relationships of species under studied. While D. venezolana and D. borborema are inhabitants of tropical deserts where environmental temperatures are warm and mostly uniform throughout the year, D. koepferae and D. buzzatii can reach areas of higher latitudes or altitudes in subtropical and temperate regions, where cold seasons likely challenges survival and fertility (Mensch et al, 2017). Climatic data from locations where the species were collected indicate that tropical and temperate species are exposed to very distinct conditions in nature (Figure S2).…”