Genetic basis of orange spot formation in the guppy (Poecilia reticulata)

Background To understand the evolutionary significance of female mate choice for colorful male ornamentation, the underlying regulatory mechanisms of such ornamentation must be understood for examining how the ornaments are associated with “male qualities” that increase the fitness or sexual attractiveness of offspring. In the guppy (Poecilia reticulata), an established model system for research on sexual selection, females prefer males possessing larger and more highly saturated orange spots as potential mates. Although previous studies have identified some chromosome regions and genes associated with orange spot formation, the regulation and involvement of these genetic elements in orange spot formation have not been elucidated. In this study, the expression patterns of genes specific to orange spots and certain color developmental stages were investigated using RNA-seq to reveal the genetic basis of orange spot formation. Results Comparing the gene expression levels of male guppy skin with orange spots (orange skin) with those without any color spots (dull skin) from the same individuals identified 1102 differentially expressed genes (DEGs), including 630 upregulated genes and 472 downregulated genes in the orange skin. Additionally, the gene expression levels of the whole trunk skin were compared among the three developmental stages and 2247 genes were identified as DEGs according to color development. These analyses indicated that secondary differentiation of xanthophores may affect orange spot formation. Conclusions The results suggested that orange spots might be formed by secondary differentiation, rather than de novo generation, of xanthophores, which is induced by Csf1 and thyroid hormone signaling pathways. Furthermore, we suggested candidate genes associated with the areas and saturation levels of orange spots, which are both believed to be important for female mate choice and independently regulated. This study provides insights into the genetic and cellular regulatory mechanisms underlying orange spot formation, which would help to elucidate how these processes are evolutionarily maintained as ornamental traits relevant to sexual selection.

Breeding displacement in gray wolves (Canis lupus): Three males usurp breeding position and pup rearing from a neighboring pack in Yellowstone National Park

Gray Wolves (Canis lupus) are territorial, group living carnivores that live in packs typically consisting of a dominant breeding pair and their offspring. Breeding tenures are relatively short and competitive, with vacancies usually occurring following a breeder’s death, and are often filled by unrelated immigrants or by relatives of the previous breeder. The frequency and conditions of active breeder displacements are poorly understood. Position changes in the dominance hierarchy are common yet rarely documented in detail. We describe a turnover in male breeding position in a wolf pack by males from a neighboring pack in mid-summer 2016 in Yellowstone National Park. Over the course of two months, three males from the Mollie’s pack displaced the breeding male of the neighboring Wapiti Lake pack, joined the pack’s two adult females, and subsequently raised the previous male’s four approximately three-month old pups. In the four years following the displacement (2017 to 2020), at least one of the intruding males has successfully bred with the dominant female and most years with a subordinate female (who was one of the pups at the time of displacement). The pack reared pups to adulthood each year. Male breeding displacements are likely influenced by male-male competition and female mate choice. These changes are the result of individuals competing to improve breeding position and may lead to increased pack stability and greater reproductive success. We report in detail on the behavior of a closely observed breeding displacement and we discuss the adaptive benefits of the change.

Mating behaviour, mate choice and female resistance in the bean flower thrips (Megalurothrips sjostedti)

Many species of thrips (Thysanoptera) in the family Thripidae form mating aggregations, but the adaptive significance of these aggregations and the extent of male and female mate choice is poorly understood. We studied the mating behaviour of the bean flower thrips Megalurothrips sjostedti (Trybom) (Thysanoptera: Thripidae), which forms male aggregations and occurs across sub-Saharan Africa. We tested whether males choose mates by female age or mating status. No-choice mating bioassays with one male and one female were used to simulate the way males usually encounter only one female at a time in aggregations in the field. Virgin females violently resisted mating attempts by males, but we found no compelling evidence to establish whether this was indiscriminate or was screening suitable males. Younger males (1–2 days old) did not discriminate females by age (1–2 or 7–10 days old), but older males (7–10 days old) avoided mating with older females. Any male choice by female mating status (virgin or mated) was weak or absent. The mating behaviour of M. sjostedti shows broad similarities with that of other thrips species that form aggregations, but also shows some distinct and novel differences, which can help our understanding of the adaptive significance of aggregations.

A supergene in seaweed flies modulates male traits and female perception

Supergenes, tightly linked allelic combinations that underlie complex adaptive phenotypes represent a critical mechanism protecting intra-specific polymorphism. Supergenes represent some of the best examples of balancing selection in nature and there is increasing evidence that disassortative mating, when individuals preferentially mate with dissimilar phenotypes, is a key force stabilizing supergene polymorphisms. Yet, the underlying biological mechanisms and genetic basis of disassortative mating remain poorly known. Here, we examine a possible mechanism of disassortative mating driven by female mate choice in relation to the overdominant Cf-Inv(1) supergene in the seaweed fly Coelopa frigida by investigating chemical communication and its genomic architecture. We show that Cf-Inv(1) strongly affects chemical signaling; cuticular hydrocarbon (CHC) composition differed between genotypes in males but not females across two continents. In tandem, Cf-Inv(1) affected female perception of these compounds; females are able to sense 36 compounds from the male CHC cocktail but show differential perception between genotypes for almost half of them. This indicates that the genetic underpinnings of male traits and female perceptions are tightly linked within Cf-Inv(1) which likely facilitates disassortative mating. A differential expression approach based on candidate genes for CHC biosynthesis and odorant detection revealed differential expression for CHC biosynthesis in males alone but broad changes in odorant receptors across both sexes. Furthermore, odorant genes clustered together within Cf-Inv(1), with some of them differing between arrangements by 8.3% at the protein level, suggesting evolution via tandem duplication then divergence. We propose that the tight linkage between overdominant loci, male traits, and female perception has helped to maintain the Cf-Inv(1) polymorphism across its range in the face of supergene degeneration.

Mate choice for major histocompatibility complex (MHC) complementarity in the Yellow-rumped Flycatcher (Ficedula zanthopygia)

Background Genes of the major histocompatibility complex (MHC) are an important component of the vertebrate immune system and play a significant role in mate choice in animal populations. However, the MHC genetic targets of female mate choice have not been clearly identified, and whether female mate choice is based on neutral genetic characteristics remains an open question. Here, we focus on the effects of morphological traits and genetic similarity among individuals in MHC class IIB (MHC IIB) exon 2 on mating in a sexually dimorphic songbird that exhibits social monogamy with extra-pair paternity (EPP). Methods We sequenced 64 parent–offspring triads sampled over a 3-year period using two MHC class II loci to detect disassortative mating in the Yellow-rumped Flycatcher (Ficedula zanthopygia). Results We found that MHC similarity in social pairs was lower than that in random pairs. Extra-pair mate choice according to MHC IIB was observed, in which females’ extra-pair mates had fewer MHC alleles than their within-pair mates, but there was no significant band-sharing between extra-pair sires and potential extra-pair mates. However, the interaction between the MHC diversity of females and that of the social males affected the occurrence of EPP. Conclusions Our results support the “optimality hypothesis” of MHC-based social and extra-pair choice. Female choice probably maintains a certain level of MHC diversity in offspring in the Yellow-rumped Flycatcher.

The dark-ventral-patch of male red deer, a sexual signal that conveys the degree of involvement in rutting behavior

Background In polygynous mammals, signalling may play a decisive role in mating behavior, mediating the intensity of male fights and female mate choice. During the rutting season, male red deer may show a visible dark patch in their ventral fur. Recently, this patch has been suggested to act as a flexible sexual signal, due to its relationships with other variables such as age, body size, antler development, volatile compounds, or the competitive environment. The analysis of fur pigmentation at the ventral patch suggests that this might also visually indicate the male intrinsic predisposition to take part in mating competition. Results To assess the possible role of this trait as a communicative signal related to mate competition, we used red deer behavioral observations during the rut in Doñana National Park (Spain) to examine the link between the degree of expression of the dark ventral patch and the rutting activity (assessed from both intra-and-inter-sexual behaviors). Consistent with our predictions, we found in a field study that males with large dark patches showed a higher frequency of rutting behaviors (mainly roaring and flehmen), more interactions with females, and attained larger harem sizes. Conclusions The dark ventral patch was a better predictor of male behavior than antler tines or territory holding, thus standing as a short-term indicator of male willingness to invest in mating competition.

Runaway evolution from male-male competition

Understanding why and how elaborated traits evolve remains a fascination and a challenge. Darwin proposed both male-male competition and female mate choice as explanations for elaboration because such traits are often mediators of social interactions that govern access to mates. Although we have robust evolutionary quantitative genetic models for how mate choice can lead to runaway evolution, we lack an equivalent framework for understanding how male-male competition can drive extreme elaboration of traits. Here, we integrate the logic of optimality models into the quantitative genetic framework of interacting phenotypes to fill this gap. We assume that males modulate their aggression based on the relative size of a trait that signals willingness and ability to fight and identify conditions where the signal undergoes rapid and exponential evolution. Males receive fitness benefits from winning contests, but they may accrue fitness costs due to threats imposed by their opponent. This cost leads to a force of social selection that accelerates as the signaling trait is elaborated, which may cause runaway evolution of the signal. Even when a runaway is checked by natural selection, we find that signaling traits evolving by male-male competition can be elaborated well beyond their naturally selected optimum. Our model identifies simple conditions generating feedback between the behavioral and morphological traits mediating male-male competition, providing clear testable predictions. We conclude that, like the well-characterized case of female mate choice, male-male competition can provide a coevolving source of selection that can drive a runaway process resulting in evolution of elaborate traits.

Glucocorticoid-mediated changes in male green treefrog vocalizations alter attractiveness to females

Adrenal glucocorticoids are increasingly recognized as important modulators of male courtship signals, suggesting that circulating levels of these steroids can play a central role in sexual selection. However, few studies have examined whether glucocorticoid-mediated effects on male sexual signals actually impact mate choice by females. Here, we examine how corticosterone (CORT)-mediated changes in the vocalizations of male green treefrogs, Dryophytes cinereus, influence attractiveness to females. In this species, agonistic acoustic signaling between rival males competing for mates increases circulating CORT levels in contest losers. Acute elevations in CORT, in turn, decrease the duration of male advertisement calls and increase the latency between successive calls, resulting in a net reduction in vocal effort (the amount of signaling per unit time) that occurs independently of changes in circulating androgens. Based on known preferences for acoustic features in D. cinereus, and other anuran species, the direction of CORT-mediated effects on temporal call characteristics are expected to compromise attractiveness to females, but whether they are of sufficient magnitude to impact female mate choice decisions is unclear. To examine whether CORT-mediated effects on male advertisement calls reduce attractiveness to females, we broadcast vocalizations in dual speaker playback experiments approximating the mean and 1SD above and below the mean call duration and vocal effort values (the two primary vocal features impacted by elevated CORT) of males with low and high CORT levels. Results revealed strong preferences by females for the calls characteristic of males with low CORT in tests using the approximate mean and 1SD above the mean call duration and vocal effort values, but females did not show a preference for calls of males with low CORT in trials using call values approximating 1SD below the mean. Overall, females preferred males with signal traits predictive of low CORT, however this effect was nonlinear with attenuated preferences when signal alternatives differed only marginally indicating a possible thresholding effect. Specifically, females appeared to discriminate between males with low vs. high CORT based primarily on differences in call rates associated with CORT-mediated changes in call duration and vocal effort. Our results highlight that changes in circulating CORT during male-male vocal interactions can decrease attractiveness to females, suggesting that circulating levels of CORT can play a critical role in both intra- and intersexual selection.