Evolution of Reproductive Behavior

Abstract

Behaviors associated with reproduction are major contributors to the evolutionary success of organisms and are subject to many evolutionary forces, including natural and sexual selection, and sexual conflict. Successful reproduction involves a range of behaviors, from finding an appropriate mate, courting, and copulation, to the successful production and (in oviparous animals) deposition of eggs following mating. As a consequence, behaviors and genes associated with reproduction are often under strong selection and evolve rapidly. Courtship rituals in flies follow a multimodal pattern, mediated through visual, chemical, tactile, and auditory signals. Premating behaviors allow males and females to assess the species identity, reproductive state, and condition of their partners. Conflicts between the "interests" of individual males, and/or between the reproductive strategies of males and females, often drive the evolution of reproductive behaviors. For example, seminal proteins transmitted by males often show evidence of rapid evolution, mediated by positive selection. Postmating behaviors, including the selection of oviposition sites, are highly variable and Drosophila species span the spectrum from generalists to obligate specialists. Chemical recognition features prominently in adaptation to host plants for feeding and oviposition. Selection acting on variation in pre-, peri-, and postmating behaviors can lead to reproductive isolation and incipient speciation. Response to selection at the genetic level can include the expansion of gene families, such as those for detecting pheromonal cues for mating, or changes in the expression of genes leading to visual cues such as wing spots that are assessed during mating. Here, we consider the evolution of reproductive behavior in Drosophila at two distinct, yet complementary, scales. Some studies take a microevolutionary approach, identifying genes and networks involved in reproduction, and then dissecting the genetics underlying complex behaviors in D. melanogaster Other studies take a macroevolutionary approach, comparing reproductive behaviors across the genus Drosophila and how these might correlate with environmental cues. A full synthesis of this field will require unification across these levels.

Keywords: Drosophila; FlyBook; adaptation; chemoreception; courtship; fitness; genetics; gene–environment interaction; mating; multigene family; natural variation; pheromones; postmating behaviors; selection; seminal proteins; song; wing spots.

Figure 1

A diagram showing the sequence of behaviors during courtship in D. melanogaster. Orienting (a), tapping (b), ‘singing (c), licking (d), attempting copulation (e), and copulation (f). Reprinted, with permission, from Sokolowski (2001).

Figure 2

Phylogenetic distribution of reproductive behaviors and associated morphologies in species groups of Drosophila. All terminal taxa represent species groups [for definitions see Markow and O’Grady (2005) and O’Grady and DeSalle (2018)]. AMC indicates the antopocerus-modified tarsus clade; PNA indicates the picture wing-nudidrosophila-ateledrosophila clade. Open squares denote missing information. Characters that are polymorphic within a group show multiple colors. Sexual dimorphism (present, green with horizontal line; absent, black). Dimorphic characters, observed in males, include wings (W), forelegs (L), mouthparts (M), and head broadening (H). Wing spreading (present, green with horizontal line; absent, black). Wing pigment (present, green with horizontal line; absent, black; polymorphic, both). Lek behavior (present, green with horizontal line; absent, black). Male guarding (present, green with horizontal line; absent, black). Reproductive maturity in males and females (0–5 days, red with diagonal line; 6–10 days, green with horizontal line; 11–15 days, orange with vertical line, > 15 days, blue with dot). Sperm size [< 6 mm (short), red with diagonal line; > 6 mm (giant), blue with dot]. Ovariole numbers (< 25, red with diagonal; > 25, blue with dot). Female remating frequency (frequent, red with diagonal line; infrequent, blue with dot). Copulation duration (< 20 min, red with diagonal line; 20–60 min, green with horizontal line; > 60 min, orange with vertical line). Insemination reaction (none, red with diagonal line; moderate, green with horizontal line; strong, orange with vertical line).

Figure 3

Lineage-specific gene loss and gain in the Or family. Diagram that illustrates gene-loss events (red slashes) and duplications (blue dots) in the melanogaster subgroup, including D. simulans (sim), D. sechellia (sec), D. melanogaster (mel), D. yakuba (yak), and D. erecta (ere). Generalist lineages are shown by solid black lines and specialist lineages by dotted lines. The timing of events was inferred via parsimony [modified from McBride et al. (2007), with permission].