Nuptial feeding encompasses any form of nutrient transfer from the male to the female during or directly after courtship and/or copulation. In insects, nuptial gifts may take the form of food captured or collected by the male, parts, or even the whole of the male's body, or glandular products of the male such as salivary secretions, external glandular secretions, the spermatophore and substances in the ejaculate. Over the past decade, there has been considerable debate over the current function of nuptial feeding in insects. This debate has centred on the issue of whether nuptial gifts function as paternal investment (i.e. function to increase the fitness and/or number of the gift-giving male's own offspring) or as mating effort (i.e. function to attract females, facilitate coupling, and/or to maximize ejaculate transfer), although the two hypotheses are not mutually exclusive. In the present article, evidence for the potential of nuptial gifts to function as either paternal investment, mating effort, or both is reviewed for each form of nuptial feeding in each insect taxon for which sufficient data are available. Empirical evidence suggests that many diverse forms of nuptial feeding in different insect taxa function, at least in part, as mating effort. For example, nuptial prey and salivary masses in the Mecoptera, regurgitated food in Drosophila (Diptera), hind-wing feeding in Cyphoderris (Orthoptera) and the secretion of the male's cephalic gland in Neopyrochroa (Coleoptera) and Zorotypus (Zoraptera) appear to function to entice females to copulate and/or to facilitate coupling. Nuptial prey and salivary masses in the Mecoptera also appear to function to maximize ejaculate transfer (which is also a form of mating effort), as do nuptial prey in Empis (Diptera), external glandular secretions in Oecanthus and Allonemobius (Orthoptera) and the spermatophylax in gryllids and tettigoniids (Orthoptera). Large spermatophores in, for example, the Lepidoptera and Coleoptera, also appear to be maintained by selection on the male to maximize ejaculate transfer and thereby counter the effects of sperm competition. In contrast to the large amount of evidence in support of the mating effort hypothesis, there is a relative lack of good evidence to support the paternal investment hypothesis. Certain studies have demonstrated an increase in the weight and/or number of eggs laid as a result of the receipt of larger gifts, or a greater number of gifts, in tettigoniids, gryllids, acridids, mantids, bruchid beetles, drosophilids and lepidopterans. However, virtually all of these studies (with the possible exception of studies of the spermatophylax in tettigoniids) have failed to control adequately for hormonal substances in the ejaculate that are known to affect female reproductive output. Furthermore, in at least four tettigoniids (but not in the case of two species), three lepidopterans, a drosophilid and probably also bruchid beetles and bittacids, evidence suggests that the male has a low probability of fertilising the eggs that stand to benefit from his nuptial gift nutrients. Therefore, the hypothesis that paternal investment might account for the function of nuptial gifts in general is not supported.

The function of nuptial feeding in insects: a review of empirical studies

Sexual selection has resulted in some of the most captivating features of insects, including flashy colors, bizarre structures, and complex pheromones. These features evolve in dynamic environments, where conditions can change rapidly over space and time. However, only recently has ecological complexity been embraced by theory and practice in sexual selection. We review replicated selection studies as well as studies on variation in the agents of selection to delineate gaps in current knowledge and clarify exciting new directions for research. Existing work suggests that fluctuations in sexual selection may be extremely common, though work on the ecological factors influencing these fluctuations is scarce. We suggest that deeper ecological perspectives on sexual selection may alter some of the fundamental assumptions of sexual selection theory and rapidly lead to new discoveries.

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Sexual Selection in Complex Environments

Manipulation of the frequency of naturally occurring colour patterns within replicate pools of fish at three sites shows that males with rare colour patterns have higher reproductive fitness, demonstrating negative frequency-dependent selection mediated by sexual selection. Given that natural selection is both ubiquitous and remorseless, how is it that variation is maintained in populations? This pressing question in evolutionary biology is answered by Kimberly Hughes and colleagues in a study of guppies (Poecilia reticulata), a particularly useful model system because guppy male colouration is one of the most genetically variable organismal traits known. It was shown previously that in a population of brightly coloured guppies, males with rare colour patterns tend to thrive, against expectation. Hughes et al. show, using carefully controlled wild populations, not only that female guppies prefer to mate with these rare males, but that the males produce more offspring than those of more common stripe. This phenomenon, known as negative frequency-dependent selection, shows that there is a price on exclusivity and provides a mechanism for maintaining variation in a population. To understand the processes that maintain genetic diversity is a long-standing challenge in evolutionary biology, with implications for predicting disease resistance, response to environmental change, and population persistence1,2,3. Simple population genetic models are not sufficient to explain the high levels of genetic diversity sometimes observed in ecologically important traits2. In guppies (Poecilia reticulata), male colour pattern is both diverse and heritable, and is arguably one of the most extreme examples of morphological polymorphism known4,5. Negative frequency-dependent selection (NFDS), a form of selection in which genotypes are favoured when they are rare6, can potentially maintain such extensive polymorphism, but few experimental studies have confirmed its operation in nature7,8. Here we use highly replicated experimental manipulations of natural populations to show that males with rare colour patterns have higher reproductive fitness, demonstrating NFDS mediated by sexual selection. Rare males acquired more mates and sired more offspring compared to common males and, as previously reported, had higher rates of survival8. Orange colour, implicated in other studies of sexual selection in guppies, did predict male reproductive success, but only in one of three populations. These data support the hypothesis that NFDS maintains diversity in the colour patterns of male guppies through two selective agents, mates and predators. Similar field-based manipulations of genotype frequencies could provide a powerful approach to reveal the underlying ecological and behavioural mechanisms that maintain genetic and phenotypic diversity.

Mating advantage for rare males in wild guppy populations

Polymorphic species, in which multiple variants coexist within a population, are often used as model systems in evolutionary biology. Recent research has been dominated by the hypothesis that polymorphism can be a precursor to speciation. To date, the majority of research regarding polymorphism and speciation has focused on whether polymorphism is maintained within a population or whether morphs within populations may diverge to form separate species (sympatric speciation); however, the geographical context of speciation in polymorphic systems is likely to be both diverse and complex. In this review, we draw attention to the geographic variation in morph composition and frequencies that characterises many, if not most polymorphic species. Recent theoretical and empirical developments suggest that such variation in the number, type and frequency of morphs present among populations can increase the probability of speciation. Thus, the geographical context of a polymorphism requires a greater research focus. Here, we review the prevalence, causes and evolutionary consequences of geographic variation in polymorphism in colour-polymorphic animal species. The prevalence and nature of geographic variation in polymorphism suggests that polymorphism may be a precursor to and facilitate speciation more commonly than appreciated previously. We argue that a better understanding of the processes generating geographic variation in polymorphism is vital to understanding how polymorphism can promote speciation.

Geographic variation in animal colour polymorphisms and its role in speciation

Genetic colour polymorphisms are widespread across animals and often subjected to complex selection regimes. Traditionally, colour morphs were used as simple visual markers to measure allele frequency changes in nature, selection, population divergence and speciation. With advances in sequencing technology and analysis methods, several model systems are emerging where the molecular targets of selection are being described. Here, we discuss recent studies on the genetics of sexually selected colour polymorphisms, aiming at (i) reviewing the evidence of sexual selection on colour polymorphisms, (ii) highlighting the genetic architecture, molecular and developmental basis underlying phenotypic colour diversification and (iii) discuss how the maintenance of such polymorphisms might be facilitated or constrained by these. Studies of the genetic architecture of colour polymorphism point towards the importance of tight clustering of colour loci with other trait loci, such as in the case of inversions and supergene structures. Other interesting findings include linkage between colour loci and mate preferences or sex determination, and the role of introgression and regulatory variation in fuelling polymorphisms. We highlight that more studies are needed that explicitly integrate fitness consequences of sexual selection on colour with the underlying molecular targets of colour to gain insights into the evolutionary consequences of sexual selection on polymorphism maintenance.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/mec.12935

Sexual selection and genetic colour polymorphisms in animals

Negative frequency-dependent selection (NFDS) is one of the most powerful selective forces maintaining genetic polymorphisms in nature. Recently many prospective cases of polymorphisms by NFDS have been reported. Some of them are very complicated, although strongly supportive of the NFDS. Here we investigate NFDS in wild populations of the dimorphic damselfly Ischnura senegalensis, in which females occur as andromorphs and gynomorphs. Specifically, we (1) test fitness responses to morph frequencies, (2) built a simple population genetic model, and (3) compare the observed and predicted morph-frequency dynamics. Fitnesses of the two morphs are an inverse function of its own frequency in a population, and are about equal when their frequencies are similar. Thus the conditions necessary for NFDS are satisfied. The long-term field surveys show that the morph frequencies oscillate with a period of two generations. Morph frequencies in a small population undergo large oscillations whereas those in a large population do small oscillations. The demographic properties of the observed dynamics agree well with those of our model. This example is one of the simplest confirmed cases of NFDS maintaining genetic polymorphisms in nature.

Negative frequency-dependent selection in female color polymorphism of a damselfly.

Female reproductive success is affected by selective male harassment in the damselfly Ischnura senegalensis

The maintenance of multiple ornaments by animals can be explained when those multiple ornaments are sexually selected. However, there have been only a few studies of sexual selection on multiple ornaments. We investigated sexual selection on two ornaments, plumage coloration and white spots in the tail, in a population of Barn Swallows Hirundo rustica gutturalis in Japan. There was sexual dimorphism in throat coloration and in the size of the white spots in the tail. Males with a less saturated (colourful) throat and larger white spots in the tail bred earlier than others, indicating a mating advantage for these males. These trends are what would be expected if these ornaments were indeed sexually selected.

/pdf/mating-advantage-of-multiple-male-ornaments-in-the-barn-3n5lc0gisn.pdf

Mating Advantage of Multiple Male Ornaments in the Barn Swallow Hirundo Rustica Gutturalis

Female mate choice based on territory quality is difficult to study because territories often contain many resources, which are difficult to quantify. Here, using the barn swallow (Hirundo rustica gutturalis) breeding at an outdoor breeding site in Japan, where each male defends only a small territory containing old nests, we studied whether females choose social mates based on territory quality. Since the territories of this species contain few other resources, territory quality can easily be assessed by quantifying old nests in the territory. We made the following four observations: (1) male swallows displayed old nests in their territories to females; (2) the old nests used for the first clutch were less broken than the other old nests within the same territory; (3) territory quality, defined by the number of old nests weighted by the intactness of each old nest, predicted the productivity of the territory; and (4) males with better territories paired with females earlier, and hence bred earlier, than those with inferior territories. The relationships remained significant even after controlling for male morphological traits. Based on these results, we can infer that female swallows choose their mates based, in part, on territory quality.

/pdf/female-mate-choice-based-on-territory-quality-in-barn-3bc6qsn5p8.pdf

Female mate choice based on territory quality in barn swallows

While male mate choice behaviour has been reported in many taxa, little is known about its plasticity and evolutionary consequences. In the damselfly Ischnura senegalensis, females exhibit colour dimorphism (gynomorph and andromorph). The body colour of gynomorphs changed ontogenetically in accordance with sexual maturation, while little change occurred in andromorphs. To test the male mate choice between sexually immature and mature females of both morphs, binary choice experiments were conducted. Virgin males that were reared separately from females after emergence did not show significant preference between sexually immature and mature females for both morphs, indicating that virgin males were unable to discriminate female reproductive status. On the other hand, males that had experienced copulation with gynomorphs preferred sexually mature gynomorphs to sexually immature ones. However, males that had experienced copulation with andromorphs could not discriminate between sexually immature and mature andromorphs, probably due to the absence of significant ontogenetic change in their thoracic colour. Therefore, female body colour is an important cue for males in discriminating between sexual maturation stages. Learned mate discrimination depending on copulation experience might help males to detect potential mates effectively and avoid sexually unreceptive immature female. We finally discuss the adaptive significance of the ontogenetic colour change in females.

Mamoru Watanabe

Papers

Negative frequency-dependent selection in female color polymorphism of a damselfly.

Female reproductive success is affected by selective male harassment in the damselfly Ischnura senegalensis

Mating Advantage of Multiple Male Ornaments in the Barn Swallow Hirundo Rustica Gutturalis

Female mate choice based on territory quality in barn swallows

Male mate choice based on ontogenetic colour changes of females in the damselfly Ischnura senegalensis