Contact-Chemosensory Evolution Underlying Reproductive Isolation in Drosophila Species

Abstract

The main theme of the review is how changes in pheromone biochemistry and the sensory circuits underlying pheromone detection contribute to mate choice and reproductive isolation. The review focuses primarily on gustatory and non-volatile signals in Drosophila. Premating isolation is prevalent among closely related species. In Drosophila, preference for conspecifics against other species in mate choice underlies premating isolation, and such preference relies on contact chemosensory communications between a female and male along with other biological factors. For example, although D. simulans and D. melanogaster are sibling species that yield hybrids, their premating isolation is maintained primarily by the contrasting effects of 7,11-heptacosadiene (7,11-HD), a predominant female pheromone in D. melanogaster, on males of the two species: it attracts D. melanogaster males and repels D. simulans males. The contrasting preference for 7,11-HD in males of these two species is mainly ascribed to opposite effects of 7,11-HD on neural activities in the courtship decision-making neurons in the male brain: 7,11-HD provokes both excitatory and inhibitory inputs in these neurons and differences in the balance between the two counteracting inputs result in the contrasting preference for 7,11-HD, i.e., attraction in D. melanogaster and repulsion in D. simulans. Introduction of two double bonds is a key step in 7,11-HD biosynthesis and is mediated by the desaturase desatF, which is active in D. melanogaster females but transcriptionally inactivated in D. simulans females. Thus, 7,11-HD biosynthesis diversified in females and 7,11-HD perception diversified in males, yet it remains elusive how concordance of the changes in the two sexes was attained in evolution.

Keywords: central integration; doublesex; fruitless; gustatory receptors; hybrids; hydrocarbon metabolism; pheromones; premating isolation.

FIGURE 1

7,11-HD plays a key role for male mate choice in the D. melanogaster species subgroup. (A) 7,11-HD is a D. melanogaster female-specific pheromone synthesized in oenocytes as mediated by enzymes including DesatF and EloF. (B) DesatF expression is female-specific in D. melanogaster and D. sechellia, whereas it is transcriptionally inactivated in D. simulans and D. mauritiana. (C) Pathways for pheromone synthesis in D. melanogaster and D. simulans. 7-T is a monoene with a double bond at the 7th carbon whereas 7,11-HD is a diene with two double bonds each at the 7th and 11th carbon as the numbers in the compound names indicate.

FIGURE 2

D. melanogaster males are attracted and D. simulans males are repelled by 7,11-HD. (A) Contrasting responses to 7,11-HD underlie conspecific mate choice. (B) F-cell and M-cell in the male tarsi sense female pheromones (e.g., 7,11-HD) and male pheromones (e.g., 7-T), respectively. The F-cell and M-cell both express ppk23, ppk29 and fru, while ppk25 expression is F-cell specific. (C) Central pathway for 7,11-HD perception in male flies involves ascending excitatory (+) neurons including vAB3 and PPN1, mAL inhibitory (–) interneurons, and courtship triggering P1 excitatory (+) interneurons. (D) mAL-mediated inhibition overwhelms vAB3-mediated excitation in P1 neurons in D. simulans males but not D. melanogaster males, resulting in opposite responses to 7,11-HD in males of these two species. P1 represents a male-specific subset in the pC1 neuron group (circled by a dotted line). Circles, lines, and triangles indicate somata, neurites, and presynaptic terminals of neurons, respectively.

FIGURE 3

Combination of several GRs expressed in a single neuron determines the response spectrum of the cell. Upper left-side panel: Spatial localization of bitter-responsive I-a (blue) and I-b (red) sensilla on the labellum. Right-side panels: The bitter-responsive neuron (labeled as “B”) of each sensillum expresses a different combination of Gustatory receptors (Grs), five of which are referred to as “Commonly Expressed Receptors” (CERs; in dotted rectangles) and are expressed in every bitter-responsive neuron on the labellum. Expression of Gr32a, Gr33a, and Gr39a.a together confers a berberine sensitivity on the I-a sensillum, whereas expression of Gr33a, Gr39a.a, Gr66a, and Gr93a together confers a caffeine sensitivity on the I-b sensillum. However, the latter four Grs are unable to confer a caffeine sensitivity on the I-a sensillum, because Gr32a, Gr59b, and Gr89a are coexpressed in this sensillum.