Extended lifespan and sex-specific fertility loss in cold-acclimated flies of the sibling species Drosophila buzzatii and Drosophila koepferae.

Survival and reproduction are the core elements of Darwinian fitness. In the context of a fixed energy budget, organisms tend to allocate resources in order to maximize one at the expense of the other, in what has been called the lifespan-reproduction trade-off. Reproductive arrest and extended lifespan are common responses to low temperatures in many insects including fruit flies. In this study, we aim to understand the overwintering strategy of two closely-related Drosophila species with contrasting distribution ranges. We compared survival, lifespan, ovarian maturation, and reproductive output (fecundity and fertility) of virgin and mated adults of both Drosophila buzzatii and Drosophila koepferae after long-term cold exposure at dormancy-inducing conditions (10 °C, 10:14 L:D) and controls (25 °C, 12:12 L:D). Virgin flies of D. buzzatii showed the longest lifespan (averaging 102 days) under dormancy-inducing conditions. Cold-induced reproductive arrest preserves reproductive capacity mainly in virgin females that mated after reproductive dormancy, indicating that males were much more susceptible to fertility loss than females, in both species. Notably, females of D. buzzatii were capable of protecting stored sperm from cold damage and produced viable progeny. Even if, in D. buzzatii, fertility of flies mated after the cold-exposure was extremely low, cold temperature likely sterilized D. koepferae males, indicating that cold carry-over effects are stronger for the species with the shorter lifespan. Such species-specific effects of low temperature over fitness likely contributed to the divergence of these closely-related species and to the spread of D. buzzatii into cooler environments.

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

Temperate species, contrary to their tropical counterparts, are exposed not only to thermally variable environments with low temperatures but also to long winters. Different selective pressures may have driven divergent physiological adaptations in closely related species with different biogeographic origins. To survive unfavourable winter conditions, Drosophila species in temperate areas generally undergo a period of reproductive dormancy, associated with a cold-induced cessation of oogenesis and metabolic reorganization. This work aims to compare cold tolerance and metabolic signatures of cold-exposed females exhibiting different reproductive maturity status (mature and immature females) of four Drosophila species from tropical vs. temperate origins. We expected that the capacity for delayed reproduction of immature females could result in the redirection of the energy-related metabolites to be utilized for surviving the cold season. To do so, we studied an array of 45 metabolites using quantitative target GC-MS profiling. Reproductively immature females of temperate species showed the lower CTmin and the faster chill coma recovery time (i.e. the most cold-tolerant group). Principal component analysis captured differences across species, but also between reproductive maturity states. Notably, temperate species exhibited significantly higher levels of glucose, alanine, and gluconolactone than tropical ones. As proline and glycerol showed higher abundances in immature females of temperate species compared to the levels exhibited by the rest of the groups, we reasoned that glucose and alanine could serve as intermediates in the synthesis of these compatible solutes. All in all, our findings suggest that cold-exposed females of temperate species accumulate energy-related and protective metabolites (e.g. glycerol and proline) while delaying reproduction, and that these metabolites are relevant to cold tolerance even at modest concentrations.

Testing the metabolic homeostasis hypothesis in amphibians.

A number of hypotheses about compensatory mechanisms that allow ectothermic animals to cope with the latitudinal decrease in ambient temperature ( TA) have been proposed during the last century. One of these hypotheses, the 'metabolic homeostasis' hypothesis (MHH), states that species should show the highest thermal sensitivity of the metabolic rate ( Q10-SMR) at the colder end of the range of TAs they usually experience in nature. This way, species should be able to minimize maintenance costs during the colder hours of the day, but quickly take advantage of increases in TA during the warmer parts of the day. Here, we created a dataset that includes Q10-SMR values for 58 amphibian species, assessed at four thermal ranges, to evaluate three predictions derived from the MHH. In line with this hypothesis, we found that: (i) Q10-SMR values tended to be positively correlated with latitude when measured at lower TAs, but negative correlated with latitude when measured at higher TAs, (ii) Q10-SMR measured at lower TAs were higher in temperate species, whereas Q10-SMR measured at higher TAs were higher in tropical species, and (iii) the experimental TA at which Q10-SMR was maximal for each species decreased with latitude. This is the first study to our knowledge showing that the relationship between Q10-SMR and latitude in ectotherms changes with the TA at which Q10-SMR is assessed, as predicted from an adaptive hypothesis. This article is part of the theme issue 'Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen'.

Contrasting Plasticity in Ovariole Number Induced by A Dietary Effect of the Host Plants between Cactophilic Drosophila Species.

Under the preference-performance hypothesis, natural selection will favor females that choose oviposition sites that optimize the fitness of their offspring. Such a preference-performance relationship may entail important consequences mainly on fitness-related traits. We used the well-characterized cactus-Drosophila system to investigate the reproductive capacity in the pair of sibling species D. buzzatii and D. koepferae reared in two alternative host plants. According to our hypothesis, ovariole number (as a proxy of reproductive capacity) depends on host plant selection. Our results indicate that the capacity of D. buzzatii showed to be mild, only increasing the number of ovarioles by as much as 10% when reared in its preferred host. In contrast, D. koepferae exhibited a similar reproductive capacity across host cacti, even though it showed a preference for its primary host cactus. Our study also revealed that D. buzzatii has a larger genetic variation for phenotypic plasticity than its sibling, although ovariole number did not show clear-cut differences between species. We will discuss the weak preference-performance pattern observed in these cactophilic species in the light of nutritional and toxicological differences found between the natural host plants.