Tropical to subpolar gradient in phospholipid composition suggests adaptive tuning of biological membrane function in drosophilids

Abstract

Variation in thermal tolerance among ectotherms has often been associated with a set of structural modifications in their cell membrane that modify the membrane's physical properties to secure appropriate fluidity at different temperatures. These adaptive mechanisms have been found in some insects, including some Drosophila species, but adaptation in phospholipid fatty acid (PLFA) composition has never been examined comprehensively in a large multispecies approach that includes appropriate phylogenetic analysis. Drosophila species are found in tropical, subtropical and temperate environments and display considerable interspecific variation in thermal tolerance. Here, we measured the PLFA composition of 55 Drosophila species that have previously been characterized for their critical thermal minima (CTmin) which represents a powerful correlate of drosophilids' distribution across thermal clines. All species were reared under common garden conditions, and interspecific variance in CTmin could therefore be related to the metrics of membrane PLFA composition without confounding effects of acclimation or rearing. We hypothesized that cold-adapted species would have PLFA's with (i) shorter chain length; (ii) higher proportion of unsaturated fatty acid; (iii) higher degree of unsaturation and (iv) lower mean melting point than warm-adapted species. Following phylogenetic correction, the data support a highly significant correlation between cold tolerance and both the proportion of unsaturated fatty acid and the degree of unsaturation. Accordingly, we also found a highly significant negative correlation with the estimated mean melting point of PLFAs. Although there was no significant correlation between PLFA length and cold tolerance, the phylogenetically corrected model found PLFA parameters to explain >20% of the variation in cold tolerance when PLFA melting point and length were included. However, further functional assays are still needed to establish how these differences in chemical composition translate into functional differences of cells at low temperature. The tropical to subpolar gradient in PLFA composition found in this study suggests adaptive tuning of biological membrane function. It is noteworthy that a single measure such as PLFA composition explains more than 20% of the interspecific variance in cold tolerance. Even though PLFA composition is only one of several important physiological characteristics that relate to interspecific differences in cold tolerance, modification of membrane composition is likely an important adaptive trait in insects and perhaps invertebrates in general.