The evolution of species recognition labels in insects

The evolution of pre-zygotic reproductive isolation is a key step in the process of speciation. In many organisms, particularly insects, chemical labels are used as pheromones for species-specific mate recognition. Although an enormous body of knowledge exists regarding the patterns of pheromone chemical ecology, much less is known about the evolutionary processes that underlie the origin of new mating pheromones. Here, we examine case studies that have illuminated the origins of species-specific mating pheromones and suggest future directions for productive research. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’.

The asymmetric chemical structures of two mating pheromones reflect their differential roles in conjugation of Schizosaccharomyces pombe

In the fission yeast Schizosaccharomyces pombe, the mating reaction is controlled by two mating pheromones, M-factor and P-factor, secreted by M- and P-type cells, respectively. M-factor is a C-terminally farnesylated lipid peptide, whereas P-factor is a simple peptide. To examine whether this chemical asymmetry in the two pheromones is essential for conjugation, we constructed a mating system in which either pheromone can stimulate both M- and P-cells, and examined whether the resulting autocrine strains can mate. Autocrine M-cells responding to M-factor successfully mated with P-factor-less P-cells, indicating that P-factor is not essential for conjugation; by contrast, autocrine P-cells responding to P-factor were unable to mate with M-factor-less M-cells. The sterility of the autocrine P-cells was completely recovered by expressing the M-factor receptor. These observations indicate that the different chemical characteristics of the two types of pheromone, a lipid and a simple peptide, are not essential; however, a lipid peptide is absolutely required for successful mating. Our findings allow us to propose a model of the differential roles of M-factor and P-factor in conjugation of S. pombe.Summary statementLipid pheromone peptides secreted locally from one cell may be concentrated at the fusion site with an opposite mating-type cell, which then polarizes to enable successful conjugation in S. pombe.

Asymmetric Diversification of Mating Pheromones in Fission Yeast

In fungi, mating between partners critically depends on the molecular recognition of two peptidyl mating pheromones by their respective receptors. The fission yeast Schizosaccharomyces pombe has two mating types, Plus (P) and Minus (M), which secrete two different mating pheromones: P-factor recognized by Mam2, and M-factor recognized by Map3, respectively. Our recent study demonstrated that a few mutations in both M-factor and Map3 can trigger reproductive isolation, a cause of speciation, in S. pombe. Here we explored the mechanism underlying reproductive isolation through genetic changes of pheromones and receptors. We investigated the diversity of genes encoding the pheromones and their receptor in 150 S. pombe wild strains. Whereas the amino acid sequences of M-factor and Map3 were completely conserved, those of P-factor and Mam2 were very diverse. In addition, the P-factor gene contained varying numbers of tandem repeats of P-factor (4–8 repeats). We also explored the recognition specificity of pheromones between S. pombe (Sp) and its close relative Schizosaccharomyces octosporus (So). So-M-factor did not have an effect on S. pombe P-cells, but So-P-factor had a partial effect on S. pombe M-cells, allowing them to mate successfully. Thus, recognition of M-factor seems to be tight, whereas that of P-factor is relatively loose. Moreover, diversity of P-factor and Mam2 might be due to a P-factor-specific peptidase. Overall, the asymmetric system for pheromone recognition in yeasts seems to allow flexible adaptation to mutational changes in the combination of pheromone and receptor while maintaining tight recognition for mating partners.

Functional overlap among distinct G1/S inhibitory pathways allows robust G1 arrest by yeast mating pheromones

In budding yeast, mating pheromones arrest the cell cycle in G1 phase via a pheromone-activated Cdk-inhibitor (CKI) protein, Far1. Alternate pathways must also exist, however, because deleting the cyclin CLN2 restores pheromone arrest to far1∆ cells. Here we probe whether these alternate pathways require the G1/S transcriptional repressors Whi5 and Stb1 or the CKI protein Sic1, whose metazoan analogues (Rb or p27) antagonize cell cycle entry. Removing Whi5 and Stb1 allows partial escape from G1 arrest in far1∆ cln2∆ cells, along with partial derepression of G1/S genes, which implies a repressor-independent route for inhibiting G1/S transcription. This route likely involves pheromone-induced degradation of Tec1, a transcriptional activator of the cyclin CLN1, because Tec1 stabilization also causes partial G1 escape in far1∆ cln2∆ cells, and this is additive with Whi5/Stb1 removal. Deleting SIC1 alone strongly disrupts Far1-independent G1 arrest, revealing that inhibition of B-type cyclin-Cdk activity can empower weak arrest pathways. Of interest, although far1∆ cln2∆ sic1∆ cells escaped G1 arrest, they lost viability during pheromone exposure, indicating that G1 exit is deleterious if the arrest signal remains active. Overall our findings illustrate how multiple distinct G1/S-braking mechanisms help to prevent premature cell cycle commitment and ensure a robust signal-induced G1 arrest.