Nectar-feeding bats and birds show parallel molecular adaptations in sugar metabolism enzymes.

In most vertebrates, the demand for glucose as the primary substrate for cellular respiration is met by the breakdown of complex carbohydrates, or energy is obtained by protein and lipid catabolism. In contrast, a few bat and bird species have convergently evolved to subsist on nectar, a sugar-rich mixture of glucose, fructose, and sucrose.1-4 How these nectar-feeders have adapted to cope with life-long high sugar intake while avoiding the onset of metabolic syndrome and diabetes5-7 is not understood. We analyzed gene sequences obtained from 127 taxa, including 22 nectar-feeding bat and bird genera that collectively encompass four independent origins of nectarivory. We show these divergent taxa have undergone pervasive molecular adaptation in sugar catabolism pathways, including parallel selection in key glycolytic and fructolytic enzymes. We also uncover convergent amino acid substitutions in the otherwise evolutionarily conserved aldolase B (ALDOB), which catalyzes rate-limiting steps in fructolysis and glycolysis, and the mitochondrial gatekeeper pyruvate dehydrogenase (PDH), which links glycolysis and the tricarboxylic acid cycle. Metabolomic profile and enzyme functional assays are consistent with increased respiratory flux in nectar-feeding bats and help explain how these taxa can both sustain hovering flight and efficiently clear simple sugars. Taken together, our results indicate that nectar-feeding bats and birds have undergone metabolic adaptations that have enabled them to exploit a unique energy-rich dietary niche among vertebrates.

The fire ant social chromosome supergene variant Sb shows low diversity but high divergence from SB.

Variation in social behaviour is common, yet little is known about the genetic architectures underpinning its evolution. A rare exception is in the fire ant Solenopsis invicta: Alternative variants of a supergene region determine whether a colony will have exactly one or up to dozens of queens. The two variants of this region are carried by a pair of 'social chromosomes', SB and Sb, which resemble a pair of sex chromosomes. Recombination is suppressed between the two chromosomes in the supergene region. While the X-like SB can recombine with itself in SB/SB queens, recombination is effectively absent in the Y-like Sb because Sb/Sb queens die before reproducing. Here, we analyse whole-genome sequences of eight haploid SB males and eight haploid Sb males. We find extensive SB-Sb differentiation throughout the >19-Mb-long supergene region. We find no evidence of 'evolutionary strata' with different levels of divergence comparable to those reported in several sex chromosomes. A high proportion of substitutions between the SB and Sb haplotypes are nonsynonymous, suggesting inefficacy of purifying selection in Sb sequences, similar to that for Y-linked sequences in XY systems. Finally, we show that the Sb haplotype of the supergene region has 635-fold less nucleotide diversity than the rest of the genome. We discuss how this reduction could be due to a recent selective sweep affecting Sb specifically or associated with a population bottleneck during the invasion of North America by the sampled population.

Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins.

Variation in social behavior is common yet our knowledge of the mechanisms underpinning its evolution is limited. The fire ant Solenopsis invicta provides a textbook example of a Mendelian element controlling social organization: alternate alleles of a genetic element first identified as encoding an odorant binding protein (OBP) named Gp-9 determine whether a colony accepts one or multiple queens. The potential roles of such a protein in perceiving olfactory cues and evidence of positive selection on its amino acid sequence made it an appealing candidate gene. However, we recently showed that recombination is suppressed between Gp-9 and hundreds of other genes as part of a >19 Mb supergene-like region carried by a pair of social chromosomes. This finding raises the need to reassess the potential role of Gp-9. We identify 23 OBPs in the fire ant genome assembly, including nine located in the region of suppressed recombination with Gp-9. For six of these, the alleles carried by the two variants of the supergene-like region differ in protein-coding sequence and thus likely in function, with Gp-9 showing the strongest evidence of positive selection. We identify an additional OBP specific to the Sb variant of the region. Finally, we find that 14 OBPs are differentially expressed between single- and multiple-queen colonies. These results are consistent with multiple OBPs playing a role in determining social structure.