Differential evolutionary constraints in the evolution of chemoreceptors: a murine and human case study

Abstract

Chemoreception is among the most important sensory modalities in animals. Organisms use the ability to perceive chemical compounds in all major ecological activities. Recent studies have allowed the characterization of chemoreceptor gene families. These genes present strikingly high variability in copy numbers and pseudogenization degrees among different species, but the mechanisms underlying their evolution are not fully understood. We have analyzed the functional networks of these genes, their orthologs distribution, and performed phylogenetic analyses in order to investigate their evolutionary dynamics. We have modeled the chemosensory networks and compared the evolutionary constraints of their genes in Mus musculus, Homo sapiens, and Rattus norvegicus. We have observed significant differences regarding the constraints on the orthologous groups and network topologies of chemoreceptors and signal transduction machinery. Our findings suggest that chemosensory receptor genes are less constrained than their signal transducing machinery, resulting in greater receptor diversity and conservation of information processing pathways. More importantly, we have observed significant differences among the receptors themselves, suggesting that olfactory and bitter taste receptors are more conserved than vomeronasal receptors.

Figure 1

Mean EPI values of chemoreceptors (red) and signal transducing machinery (blue). The edges of the boxes indicate the upper and lower quartiles. The line at the center of each box indicates the median, the square represents the mean, and whiskers represent the standard deviation. Asterisks indicate statistically significant data (P < 0.001).

Figure 2

Mean EPI values of chemoreceptors families (red) and their respective signal transducing machineries (blue). Plasticity values are shown in the vertical axis and the different subgroups are listed on the horizontal axis. Whiskers represent the standard deviation. Statistically significant data are indicated by double (P < 0.001) and single (P < 0.05) asterisks.

Figure 3

Connectivity values distribution for the chemoreceptors families (red) and their respective signal transducing machineries (blue). Values are shown in the vertical axis and the different subgroups are listed in the horizontal axis.

Figure 4

Clusterization values distribution for the chemoreceptors families (red) and their respective signal transducing machineries (blue). Values are shown in the vertical axis and the different subgroups are listed in the horizontal axis.

Figure 5

Mean EPI values of chemoreceptors families. Plasticity values are shown in the vertical axis and the different families are listed on the horizontal axis. The line at the center of each box indicates the median, the square represents the mean, and whiskers represent the standard deviation. Statistically significant data are indicated by double (P < 0.001) and single (P < 0.05) asterisks.

Figure 6

Reconstructed phylogenetic tree of the chemoreceptor families. Each square represents a CR gene. Blue, red, and green squares represent Rattus norvegicus, Mus musculus, and Homo sapiens genes, respectively. Phylogenetic trees were reconstructed with Tamura-Nei model. T1R: type I taste receptors; T2R: type II taste receptors; VN: vomeronasal receptors.

Figure 7

Graphical representation of Mus musculus chemosensory network. EPI values are plotted on each node by a color scale. Higher plasticity is indicated by bluish colors and lower plasticity by reddish colors. The other networks are not shown in this paper. Nodes represent protein coding genes and edges, functional interactions.