A genetic switch for male UV iridescence in an incipient species pair of sulphur butterflies

Mating cues evolve rapidly and can contribute to species formation and maintenance. However, little is known about how sexual signals diverge and how this variation integrates with other barrier loci to shape the genomic landscape of reproductive isolation. Here, we elucidate the genetic basis of ultraviolet (UV) iridescence, a courtship signal that differentiates the males of Colias eurytheme butterflies from a sister species, allowing females to avoid costly heterospecific matings. Anthropogenic range expansion of the two incipient species established a large zone of secondary contact across the eastern United States with strong signatures of genomic admixtures spanning all autosomes. In contrast, Z chromosomes are highly differentiated between the two species, supporting a disproportionate role of sex chromosomes in speciation known as the large-X (or large-Z) effect. Within this chromosome-wide reproductive barrier, linkage mapping indicates that cis-regulatory variation of bric a brac (bab) underlies the male UV-iridescence polymorphism between the two species. Bab is expressed in all non-UV scales, and butterflies of either species or sex acquire widespread ectopic iridescence following its CRISPR knockout, demonstrating that Bab functions as a suppressor of UV-scale differentiation that potentiates mating cue divergence. These results highlight how a genetic switch can regulate a premating signal and integrate with other reproductive barriers during intermediate phases of speciation.

A genetic switch for male UV-iridescence in an incipient species pair of sulphur butterflies

Mating cues evolve rapidly and can contribute to species formation and maintenance. However, little is known about how sexual signals diverge and how this variation integrates with other barrier loci to shape the genomic landscape of reproductive isolation. Here, we elucidate the genetic basis of UV iridescence, a courtship signal that differentiates the males of Colias eurytheme butterflies from a sister species, allowing females to avoid costly heterospecific matings. Anthropogenic range expansion of the two incipient species established a large zone of secondary contact across the eastern US with strong signatures of genomic admixtures spanning all autosomes. In contrast, Z chromosomes are highly differentiated between the two species, supporting a disproportionate role of sex chromosomes in speciation known as the large-X effect. Within this chromosome-wide reproductive barrier, cis-regulatory variation of bric a brac (bab) drives the male UV-iridescence polymorphism between the two species. Bab is expressed in all non-UV scales, and butterflies of either species or sex acquire widespread ectopic iridescence following its CRISPR knock-out, demonstrating that Bab functions as a suppressor of UV-scale differentiation that potentiates mating cue divergence. These results provide new insights into the diversification of sexual signals and the species concept.

Sex differences in the development and expression of a preference for familiar vocal signals in songbirds

Production and perception of birdsong critically depends on early developmental experience. In species where singing is a sexually dimorphic trait, early life song experience may affect later behavior differently between sexes. It is known that both male and female songbirds acquire a life-long memory of early song experience, though its function remains unclear. In this study, we hypothesized that male and female birds express a preference for their fathers’ song, but do so differently depending on the developmental stage. We measured preference for their father’s song over an unfamiliar one in both male and female Bengalese finches at multiple time points across ontogeny, using phonotaxis and vocal response as indices of preference. We found that in males, selective approach to their father’s song decreased as they developed while in females, it remained stable regardless of age. This may correspond to a higher sensitivity to tutor song in young males while they are learning and a retained sensitivity in females because song is a courtship signal that is used throughout life. In addition, throughout development, males vocalized less frequently during presentation of their father’s song compared to unfamiliar song, whereas females emitted more calls to their father’s song. These findings contribute to a deeper understanding of why songbirds acquire and maintain such a robust song memory.

Male courtship signal modality and female mate preference in the wolf spider Schizocosa ocreata: results of digital multimodal playback studies

Females must be able to perceive and assess male signals, especially when they occur simultaneously with those of other males. Previous studies show female Schizocosa ocreata wolf spiders display receptivity to isolated visual or vibratory courtship signals, but increased receptivity to multimodal courtship. It is unknown whether this is true when females are presented with a choice between simultaneous multimodal and isolated unimodal male courtship. We used digital playback to present females with a choice simulating simultaneous male courtship in different sensory modes without variation in information content: 1) isolated unimodal visual versus vibratory signals; 2) multimodal versus vibratory signals; and 3) multimodal versus visual signals. When choosing between isolated unimodal signals (visual or vibratory), there were no significant differences in orientation latency and number of orientations, approaches or receptive displays directed to either signal. When given a choice between multimodal versus vibratory-only male courtship signals, females were more likely to orient to the multimodal stimulus, and directed significantly more orients, approaches and receptivity behaviors to the multimodal signal. When presented with a choice between multimodal and visual-only signals, there were significantly more orients and approaches to the multimodal signal, but no significant difference in female receptivity. Results suggest that signal modes are redundant and equivalent in terms of qualitative responses, but when combined, multimodal signals quantitatively enhance detection and/or reception. This study confirms the value of testing preference behavior using a choice paradigm, as female preferences may depend on the context (e.g., environmental context and social context) in which they are presented with male signals.

An Evaluation of the Role of Sensory Drive in the Evolution of Lake Malawi Cichlid Fishes

Although the cichlids of Lake Malawi are an important model system for the study of sensory evolution and sexual selection, the evolutionary processes linking these two phenomena remain unclear. Prior works have proposed that evolutionary divergence is driven by sensory drive, particularly as it applies to the visual system. While evidence suggests that sensory drive has played a role in the speciation of Lake Victoria cichlids, the findings from several lines of research on cichlids of Lake Malawi are not consistent with the primary tenets of this hypothesis. More specifically, three observations make the sensory drive model implausible in Malawi: (i) a lack of environmental constraint due to a broad and intense ambient light spectrum in species rich littoral habitats, (ii) pronounced variation in receiver sensory characteristics, and (iii) pronounced variability in male courtship signal characteristics. In the following work, we synthesize the results from recent studies to draw attention to the importance of sensory variation in cichlid evolution and speciation, and we suggest possible avenues of future research.

Determinants of reproductive success across sequential episodes of sexual selection in a firefly

Because females often mate with multiple males, it is critical to expand our view of sexual selection to encompass pre-, peri- and post-copulatory episodes to understand how selection drives trait evolution. In Photinus fireflies, females preferentially respond to males based on their bioluminescent courtship signals, but previous work has shown that male paternity success is negatively correlated with flash attractiveness. Here, we experimentally manipulated both the attractiveness of the courtship signal visible to female Photinus greeni fireflies before mating and male nuptial gift size to determine how these traits might each influence mate acceptance and paternity share. We also measured pericopulatory behaviours to examine their influence on male reproductive success. Firefly males with larger spermatophores experienced dual benefits in terms of both higher mate acceptance and increased paternity share. We found no effect of courtship signal attractiveness or pericopulatory behaviour on male reproductive success. Taken together with previous results, this suggests a possible trade-off for males between producing an attractive courtship signal and investing in nuptial gifts. By integrating multiple episodes of sexual selection, this study extends our understanding of sexual selection in Photinus fireflies and provides insight into the evolution of male traits in other polyandrous species.

Song, Dance, and Smell Routine? Interpreting the Content and Function of Multimodal Signals in a Songbird, the Dark-Eyed Junco (Junco Hyemalis)

The study of animal communication has been dominated by a focus on signal types that are easily recognized and quantified by human observers. This approach has inevitably limited our ability to identify cryptic signals such as low-amplitude vocalizations and signals that transmit beyond the range of our sensory system, such as most olfactory signals. Only recently with the development of new technologies and less biased sampling techniques have we begun to unravel the importance and function of these non-traditional signal types. Here we report the results of two experiments focusing on poorly studied signals using a common songbird, the dark-eyed junco. We investigated the effect of low-amplitude song on male physiology and the occurrence of bill-wiping behavior during courtship and aggressive interactions. Preliminary results suggest that males do not alter their plasma testosterone or corticosterone levels in response to a song playback of high-amplitude or low-amplitude song, indicating that a stronger stimulus may be necessary to affect circulating hormones. Males that received intrusions of a live male or female conspecific performed significantly more bill-wiping in response to the female conspecific, suggesting that bill-wiping may be an important and overlooked courtship signal in this species.