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.

Copulation Song inDrosophila: Do Females Sing to Change Male Ejaculate Allocation and Incite Postcopulatory Mate Choice?

“…If females sing in a wide range of species during copulation, it could be also of interest to study potential correlation between female song and the evolution of copulation duration, [18,127] female remating, [114] seminal fluid proteins, [128] and sperm storage organs. [36] As mentioned in the introduction, male courtship song shows large interspecific variation in patterning and the occurrence of different song types.…”

“…[14,15] Since then, a fascinating variety of over hundred species specific male precopulatory courtship songs has been reported. [16][17][18] In species of the Drosophila virilis group, females respond to male songs with their own precopulatory songs, which stimulate the male and lead to duetting behavior. [19][20][21][22] Precopulatory courtship songs serve both sex and species recognition and increase the likelihood of copulation.…”

A double negative post-transcriptional regulatory circuit underlies the virgin behavioral state

“…Mature female virgins are more receptive to male courtship and copulation, but following mating and/or pregnancy, decrease their sexual activity and modulate behaviors to generate and foster their children. Behavioral remodeling associated with the female reproductive state includes increased aggression and nest building in avians and mammals (Ogawa and Makino, 1984;Svare et al, 1982), and decreased male acceptance, increased egg-laying, and manifold appetitive and metabolic changes in insects (Anholt et al, 2020). The genetic and neurological control of this process has been intensively studied in female fruitflies, where sexual activity induces the post-mating switch, a host of behavioral changes collectively known as post-mating responses (PMRs) (Anholt et al, 2020).…”

“…Behavioral remodeling associated with the female reproductive state includes increased aggression and nest building in avians and mammals (Ogawa and Makino, 1984;Svare et al, 1982), and decreased male acceptance, increased egg-laying, and manifold appetitive and metabolic changes in insects (Anholt et al, 2020). The genetic and neurological control of this process has been intensively studied in female fruitflies, where sexual activity induces the post-mating switch, a host of behavioral changes collectively known as post-mating responses (PMRs) (Anholt et al, 2020). While some alterations of female behaviors are required for effective reproduction and/or overtly benefit progeny, her reproductive behaviors can also be modulated by the male in ways that are antagonistic to her interests (Anholt et al, 2020).…”

“…The genetic and neurological control of this process has been intensively studied in female fruitflies, where sexual activity induces the post-mating switch, a host of behavioral changes collectively known as post-mating responses (PMRs) (Anholt et al, 2020). While some alterations of female behaviors are required for effective reproduction and/or overtly benefit progeny, her reproductive behaviors can also be modulated by the male in ways that are antagonistic to her interests (Anholt et al, 2020). The fact that aspects of this regulatory program evolve under evolutionary scenarios of conflict highlights its non-intuitive operation.…”