Bruce E. Lyon

Adaptive Plasticity in Female Mate Choice Dampens Sexual Selection on Male Ornaments in the Lark Bunting

Theory on the evolution of ornamental male traits by sexual selection assumes consistency in selection over time. Temporal variation in female choice could dampen sexual selection, but scant information exists on the degree to which individual female preferences are flexible. Here we show that in lark buntings sexual selection on male traits varied dramatically across years and, in some cases, exhibited reversals in the direction of selection for a single trait. We show that these shifts are probably because of flexibility in mate choice by individual females and that they parallel shifts in the male traits that predict female reproductive success in a given year. Plasticity in choice and concomitant reversals in mating patterns across time may weaken the strength of sexual selection and could maintain genetic variation underlying multiple sexual ornaments.

The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition

Ornaments, weapons and aggressive behaviours may evolve in female animals by mate choice and intrasexual competition for mating opportunities—the standard forms of sexual selection in males. However, a growing body of evidence suggests that selection tends to operate in different ways in males and females, with female traits more often mediating competition for ecological resources, rather than mate acquisition. Two main solutions have been proposed to accommodate this disparity. One is to expand the concept of sexual selection to include all mechanisms related to fecundity; another is to adopt an alternative conceptual framework—the theory of social selection—in which sexual selection is one component of a more general form of selection resulting from all social interactions. In this study, we summarize the history of the debate about female ornaments and weapons, and discuss potential resolutions. We review the components of fitness driving ornamentation in a wide range of systems, and show that selection often falls outside the limits of traditional sexual selection theory, particularly in females. We conclude that the evolution of these traits in both sexes is best understood within the unifying framework of social selection.

Egg recognition and counting reduce costs of avian conspecific brood parasitism

Birds parasitized by interspecific brood parasites often adopt defences based on egg recognition but such behaviours are puzzlingly rare in species parasitized by members of the same species. Here I show that conspecific egg recognition is frequent, accurate and used in three defences that reduce the high costs of conspecific brood parasitism in American coots. Hosts recognized and rejected many parasitic eggs, reducing the fitness costs of parasitism by half. Recognition without rejection also occurred and some hosts banished parasitic eggs to inferior outer incubation positions. Clutch size comparisons revealed that females combine egg recognition and counting to make clutch size decisions—by counting their own eggs, while ignoring distinctive parasitic eggs, females avoid a maladaptive clutch size reduction. This is clear evidence that female birds use visual rather than tactile cues to regulate their clutch sizes, and provides a rare example of the ecological and evolutionary context of counting in animals.

DELAYED PLUMAGE MATURATION IN PASSERINE BIRDS: RELIABLE SIGNALING BY SUBORDINATE MALES?

Three hypotheses (Cryptic, Female Mimicry, and Winter Adaptation) have been proposed to explain the occurrence of delayed plumage maturation (DPM) in passerine birds. We show that each of these hypotheses is really a composite of two different questions about: 1) the proximate function of dull plumage in second year (SY) males and 2) the selective mechanism that has favored that proximate function. We review the three hypotheses in the context of this distinction, and we find little evidence clearly supporting any of them. We propose a new Status Signaling Hypothesis (SSH) suggesting that dull SY male plumage is a reliable signal of subordinate. We suggest that female choice based on male plumage color (as an index of male quality) is the selective mechanism that has favored subordinate status signaling by SY males. If females prefer bright males, then dull plumage may be a reliable signal of subordinance and SY males may experience reduced levels of aggression from adult males. Male characters (like plumage color) are most likely to be the object of female choice when males defend simple nesting territories with little or no variation in territory quality. In such a system, SY males with low resource‐holding potential would benefit (via matings or experience) by signaling subordinance and being allowed to settle among more brightly colored adults. Thus, DPM is expected to be more prevalent when males defend simple nesting territories. This prediction of the SSH is supported by data from the literature—a significantly higher proportion of species with DPM defend simple nesting territories (versus all‐purpose territories) than do species without DPM.

Incubation feeding in snow buntings: female manipulation or indirect male parental care?

SummaryMale snow buntings regularly feed their mates on the nest during the incubation period. We removed males from 7 females at the start of incubation (Early Widows) and from 7 others when the eggs hatched (Late Widows) to experimentally assess the effects of incubation feeding on the behaviour of females and the reproductive success of both parents. Early Widows spent significantly more time off their nests than Late Widows and Controls. As a consequence, Early Widows had significantly longer incubation periods and a significantly higher proportion of them lost two or more eggs during development. There was no difference between Early and Late Widows in any index of reproductive success measured during the nestling period although significantly earlier brood reduction suggests that Early Widows were in poorer condition than Late Widows. Since both parents benefitted from incubation feeding by increased hatching success and shorter incubation periods, we conclude that this behaviour is an adaptive form of indirect parental care by males and is not the result of female manipulation.

Sexual selection is a form of social selection

Social selection influences the evolution of weapons, ornaments and behaviour in both males and females. Thus, social interactions in both sexual and non-sexual contexts can have a powerful influence on the evolution of traits that would otherwise appear to be detrimental to survival. Although clearly outlined by West-Eberhard in the early 1980s, the idea that social selection is a comprehensive framework for the study of ornaments and weapons has largely been ignored. In West-Eberhards view, sexual selection is a form of social selection—a concept supported by several lines of evidence. Darwins distinction between natural and sexual selection has been useful, but recent confusion about the limits of sexual selection suggests that some traits are not easily categorized as naturally or sexually selected. Because social selection theory has much to offer the current debates about both sexual selection and reproductive competition in females, it is sometimes viewed, narrowly, to be most useful when considering female roles. However, social selection theory encompasses much more than female reproductive competition. Our goal here was to provide that broader perspective.

Disruptive sexual selection for plumage coloration in a passerine bird

The theory of sexual selection was developed to explain the evolution of highly exaggerated sexual ornaments. Now supported by vast empirical evidence, sexual selection is generally considered to favour individuals with the most extreme trait expression. Here we describe disruptive selection on a sexual ornament, plumage coloration, in yearling male lazuli buntings (Passerina amoena). In habitats with limited good-quality nesting cover, the dullest and the brightest yearlings were more successful in obtaining high-quality territories, pairing with females and siring offspring, than yearlings with intermediate plumage. This pattern reflects the way that territorial adult males vary levels of aggression to influence the structure of their social neighbourhood. Adult males showed less aggression towards dull yearlings than intermediate and bright ones, permitting the dull yearlings to settle on good territories nearby. Fitness comparisons based on paternity analyses showed that both the adults and dull yearlings benefited genetically from this arrangement, revealing a rare example of sexually selected male–male cooperation.

Male parental care and monogamy in snow buntings

SummaryWe experimentally removed males from a random sample of 14 snow bunting (Plectrophenax nivalis) pairs to determine the influence of male parental care on reproductive success. Widowed females increased their rate of food delivery to nestlings by increasing their feeding visit rate but not their load size. However, Widows were only able to achieve 73% of the food delivery rate of Control pairs and, as a result, they raised fewer offspring of lower quality (i.e. lower mass at fledging). Total brood mass raised by Widows was only 55% of that of Control pairs. Thus, in the year of our experiment, male parental care in the nestling period almost doubled the reproductive success realized from a brood. Our experiment, however, was done in a year of poor food availability and data from the previous year, when food supply was higher, indicate that males may not always be so important. Since nestling food supply appears to be unpredictable at the time of pair formation, we suggest that monogamy is a bet-hedging strategy in case of poor food availability. As a consequence the importance of male parental care in some years may explain why snow buntings are almost always monogamous.

Optimal clutch size and conspecific brood parasitism

Egg-laying organisms should lay, in a reproductive bout, the number of eggs that maximizes fitness. Lack argued 50 years ago that clutch size for most birds is limited by the amount of food parents can provide for their offspring. Clutch sizes, however, are often smaller than this ‘Lack clutch size’, and this fact is the subject of much debate. Here I propose and test a new explanation for this pattern that is based on evidence that conspecific brood parasitism is widespread in birds, specifically when females with their own nests also parasitize conspecific birds. A graphical model of clutch size shows that the trade-offs a brood parasite faces when allocating eggs to her own nest or to nests of other conspecific females can favour a reduction in the parasites own clutch size. This prediction is supported by a field study of American coots (Fulica americana). Moreover, the cost of receiving parasitic eggs also favours a reduction in clutch size for hosts, introducing a ‘game’ element to clutch size when parasitic females are themselves parasitized. These results indicate that conspecific brood parasitism should no longer be ignored as a force in clutch-size evolution.

Coots use hatch order to learn to recognize and reject conspecific brood parasitic chicks

Avian brood parasites and their hosts provide model systems for investigating links between recognition, learning, and their fitness consequences. One major evolutionary puzzle has continued to capture the attention of naturalists for centuries: why do hosts of brood parasites generally fail to recognize parasitic offspring after they have hatched from the egg, even when the host and parasitic chicks differ to almost comic degrees? One prominent theory to explain this pattern proposes that the costs of mistakenly learning to recognize the wrong offspring make recognition maladaptive. Here we show that American coots, Fulica americana, can recognize and reject parasitic chicks in their brood by using learned cues, despite the fact that the hosts and the brood parasites are of the same species. A series of chick cross-fostering experiments confirm that coots use first-hatched chicks in a brood as referents to learn to recognize their own chicks and then discriminate against later-hatched parasitic chicks in the same brood. When experimentally provided with the wrong reference chicks, coots can be induced to discriminate against their own offspring, confirming that the learning errors proposed by theory can exist. However, learning based on hatching order is reliable in naturally parasitized coot nests because host eggs hatch predictably ahead of parasite eggs. Conversely, a lack of reliable information may help to explain why the evolution of chick recognition is not more common in hosts of most interspecific brood parasites.