Protein folding and binding can emerge as evolutionary spandrels through structural coupling

Protein folding and binding can emerge as evolutionary spandrels through structural coupling

Michael Manhart, Alexandre V Morozov

Binding interactions between proteins and other molecules mediate numerous cellular processes, including metabolism, signaling, and regulation of gene expression. These interactions evolve in response to changes in the protein’s chemical or physical environment (such as the addition of an antibiotic), or when genes duplicate and diverge. Several recent studies have shown the importance of folding stability in constraining protein evolution. Here we investigate how structural coupling between protein folding and binding — the fact that most proteins can only bind their targets when folded — gives rise to evolutionary coupling between the traits of folding stability and binding strength. Using biophysical and evolutionary modeling, we show how these protein traits can emerge as evolutionary “spandrels” even if they do not confer an intrinsic fitness advantage. In particular, proteins can evolve strong binding interactions that have no functional role but merely serve to stabilize the protein if misfolding is deleterious. Furthermore, such proteins may have divergent fates, evolving to bind or not bind their targets depending on random mutation events. These observations may explain the abundance of apparently nonfunctional interactions among proteins observed in high-throughput assays. In contrast, for proteins with both functional binding and deleterious misfolding, evolution may be highly predictable at the level of biophysical traits: adaptive paths are tightly constrained to first gain extra folding stability and then partially lose it as the new binding function is developed. These findings have important consequences for our understanding of fundamental evolutionary principles of both natural and engineered proteins.

Postmating reproductive barriers contribute to the incipient sexual isolation of US and Caribbean Drosophila melanogaster

Postmating reproductive barriers contribute to the incipient sexual isolation of US and Caribbean Drosophila melanogaster

Joyce Y Kao, Seana Lymer, Sea H Hwang, Albert Sung, Sergey V Nuzhdin

The nascent stages of speciation start with the emergence of sexual isolation. Understanding how reproductive barriers influence this evolutionary process is an ongoing effort. We present here a study of Drosophila melanogaster populations from the southeast United States and Caribbean islands undergoing incipient sexual isolation. The existence of premating reproductive barriers have been previously established, but they do not fully account for the degree of isolation present. To assess the influence of postmating barriers, we investigated putative postmating barriers of female remating and egg laying behavior, as well as hatchability of eggs laid and female longevity after mating. While we did not find any effects in female remating or egg laying, we did observe lower hatchability in the central region of our geographical spread as well as shorten female life spans after mating to genetically different males in females originating from the northern- and southernmost locations of those surveyed. These results serve as evidence that long-term consequences after mating such as the fitness of offspring and shortened lifespan have a stronger effect than short-term postmating behaviors.

Sex-biased expression in the Drosophila melanogaster group

Sex-biased expression in the Drosophila melanogaster group

Rebekah L. Rogers, Ling Shao, Jaleal S. Sanjak, Peter Andolfatto, Kevin R. Thornton
(Submitted on 1 Aug 2014)

Here, we provide revised gene models for D. ananassae, D. yakuba, and D. simulans, which include UTRs and empirically verified intron-exon boundaries, as well as ortholog groups identified using a fuzzy reciprocal-best-hit blast comparison. Using these revised annotations, we perform differential expression testing using the cufflinks suite to provide a broad overview of differential expression between reproductive tissues and the carcass. We identify thousands of genes that are differentially expressed across tissues in D. yakuba and D. simulans, with roughly 60% agreement in expression patterns of orthologs in D. yakuba and D. simulans. We identify several cases of putative polycistronic transcripts, pointing to a combination of transcriptional read-through in the genome as well as putative gene fusion and fission events across taxa. We furthermore identify hundreds of lineage specific genes in each species with no blast hits among transcripts of any other Drosophila species, which are candidates for neofunctionalized proteins and a potential source of genetic novelty.

The dynamics of sperm cooperation in a competitive environment

The dynamics of sperm cooperation in a competitive environment

H. S. Fisher, L. Giomi, H. E. Hoekstra, L. Mahadevan
(Submitted on 2 Jul 2014)

Sperm cooperation has evolved in a variety of taxa and is often considered a response to sperm competition, yet the benefit of this form of collective movement remains unclear. Here we use fine-scale imaging and a minimal mathematical model to study sperm aggregation in the rodent genus Peromyscus. We demonstrate that as the number of sperm cells in an aggregate increase, the group moves with more persistent linearity but without increasing speed; this benefit, however, is offset in larger aggregates as the geometry of the group forces sperm to swim against one another. The result is a non-monotonic relationship between aggregate size and average velocity with both a theoretically predicted and empirically observed optimum of 6-7 sperm/aggregate. To understand the role of sexual selection in driving these sperm group dynamics, we compared two sister-species with divergent mating systems and find that sperm of P.maniculatus (highly promiscuous), which have evolved under intense competition, form optimal-sized aggregates more often than sperm of P.polionotus (strictly monogamous), which lack competition. Our combined mathematical and experimental study of coordinated sperm movement reveals the importance of geometry, motion and group size on sperm velocity and suggests how these physical variables interact with evolutionary selective pressures to regulate cooperation in competitive environments.

A field test for frequency-dependent selection on mimetic colour patterns in Heliconius butterflies

A field test for frequency-dependent selection on mimetic colour patterns in Heliconius butterflies

Patricio Alejandro Salazar Carrión, Martin Stevens, Robert T. Jones, Imogen Ogilvie, Chris Jiggins

Müllerian mimicry, the similarity among unpalatable species, is thought to evolve by frequency-dependent selection. Accordingly, phenotypes that become established in an area are positively selected because predators have learnt to avoid these forms, while introduced phenotypes are eliminated because predators have not yet learnt to associate these other forms with unprofitability. We tested this prediction in two areas where different colour morphs of the mimetic species Heliconius erato and H. melpomene have become established, as well as in the hybrid zone between these morphs. In each area we tested for selection on three colour patterns: the two parental and the most common hybrid. We recorded bird predation on butterfly models with paper wings, matching the appearance of each morph to bird vision, and plasticine bodies. We did not detect differences in survival between colour morphs, but all morphs were more highly attacked in the hybrid zone. This finding is consistent with recent evidence from controlled experiments with captive birds, which suggest that the effectiveness of warning signals decreases when a large signal diversity is available to predators. This is likely to occur in the hybrid zone where over twenty hybrid phenotypes coexist.