Robert Montgomerie

RISKS AND REWARDS OF NEST DEFENCE BY PARENT BIRDS

Nest and offspring defence by birds can be treated as an optimization problem wherein fitness benefits are determined by the survival of the current brood and fitness costs depend upon the probability that the parent will survive to breed again. At the optimal intensity of defence, net fitness benefits are maximized. Unlike many other aspects of animal behavior, the reproductive consequences of nest defence can often be measured directly. Within this optimality framework, we review the current adaptive hypotheses to explain both interspecific and intraspecific variation in nest defence behavior, and we present some new ideas of our own. Most research to date has focused on seasonal patterns of nest defence to test the prediction that the intensity of nest defence should increase through the nesting cycle either because renesting potential declines or because the probability of offspring survival increases rapidly relative to that of the parents. Studies testing the renesting potential hypothesis have both supported and rejected it, but few studies to date have been controlled well enough to allow us to distinguish between the two hypotheses. The intensity of nest defence is also predicted to increase with parental experience and confidence of parenthood; offspring number, quality and vulnerability; and nest accessibility and conspicuousness. The response of parents is also expected to vary with the relative armament and mobility of parent and predator and the relative roles of the parents in caring for their offspring. Although there is some evidence supporting many of these predictions, most have not been explicitly tested while holding other factors constant. The tendency for researchers to ignore variables that might influence the intensity of nest defence makes the conclusions of most studies that find support for any single adaptive hypothesis relatively unconvincing. Like Optimal Foraging Theory, however, a comprehensive functional theory of nest defence based on life-history theory can help us to elucidate many of the patterns observed in this important aspect of the parental care behavior of a wide variety of animals.

Plumage colour signals nutritional condition in the house finch

Many animal species have bright, carotenoid-based integumentary coloration that is an important criterion in female choice. It has generally been assumed that carotenoid-based colour displays act as signals of quality because they reflect the foraging ability of the bearer, but this hypothesis has not been tested. In birds, carotenoid pigmentation of feathers is deposited at the time of moult. During moult, feathers grow in regular daily cycles resulting in ‘growth bars’ that provide a record of the rate of feather growth. To test the idea that the brightness of carotenoid coloration reflects nutritional condition during moult, we compared the brightness of carotenoid-based plumage coloration with both feather growth rate and timing of moult in male house finches (Carpodacus mexicanus). Among four populations with substantial differences in mean male plumage brightness, there was no significant variation in mean feather growth rate. Thus, the reduced brightness of some populations is not the result of reduced access to food per se. Within populations, we found a significant positive relation between the growth rate of a male’s tail feathers and the brightness of his plumage, suggesting that males growing brighter feathers are in better nutritional condition. The growth rate of tail feathers of captive males provided with ad libitum food was also significantly greater than the growth rate of males in any wild populations. Within populations, we also found a significant negative relation between the onset of moult and plumage colour, with males growing brighter feathers starting moulting earlier. These observations provide support for the hypothesis that carotenoid-based plumage coloration is an indicator of nutritional condition during moult. Variation in nutritional condition may arise from differences among individuals in either their foraging ability or their health.

Mortality costs of sexual dimorphism in birds

Sexually selected traits provide a mating advantage to the bearer but they should also exact a cost through natural selection. Whereas the mating benefits from such traits have been well documented, the costs have been difficult to demonstrate. In this analysis of mortality patterns across 28 North American passerine bird species, we show that sex-biased mortality (log10 male mortality – log10 female mortality) is positively correlated with both sexual size dimorphism and male plumage brightness. Male (but not female) mortality is positively correlated with sexual size dimorphism, suggesting a cost to male–male competition. Female (but not male) mortality is negatively correlated with male brightness, and we argue from this that the evolution of male brightness has been constrained by mortality costs. Thus sexual dimorphism in body size and plumage colour within bird species appears to be influenced by the opposing forces of sexual selection, acting to increase dimorphism, and adult mortality rates, which constrain the evolution of these traits. Differences in the expression of ornamental traits across species may be explained not only by variation in the mating benefits that accrue from ornaments, as is so often assumed, but also by variation in the costs of these traits.

Dietary carotenoids predict plumage coloration in wild house finches

Carotenoid pigments are a widespread source of ornamental coloration in vertebrates and expression of carotenoid–based colour displays has been shown to serve as an important criterion in female mate choice in birds and fishes. Unlike other integumentary pigments, carotenoids cannot be synthesized; they must be ingested. Carotenoid–based coloration is condition–dependent and has been shown to be affected by both parasites and nutritional condition. A controversial hypothesis is that the expression of carotenoid–based coloration in wild vertebrates is also affected by the amount and types of carotenoid pigments that are ingested. We tested this carotenoid-limitation hypothesis by sampling the gut contents of moulting house finches and comparing the concentration of carotenoid pigments in their gut contents with the colour of growing feathers. We found a positive association: males that ingested food with a higher concentration of carotenoid pigments grew brighter ornamental plumage. We also compared the concentration of carotenoids in the gut contents of males from two subspecies of house finches with small and large patches of carotenoid–based coloration. Consistent with the hypothesis that carotenoid access drives the evolution of carotenoid-based colour displays, males from the population with limited ornamentation had much lower concentrations of carotenoids in their gut contents than males from the population with extensive ornamentation. These observations support the idea that carotenoid intake plays a part in determining the plumage brightness of male house finches.

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.

THE EVOLUTION OF SPERM SIZE IN BIRDS

Sperm size varies enormously among species, but the reasons for this variation remain obscure. Since it has been suggested that swimming velocity increases with sperm length, earlier studies proposed longer (and therefore faster) sperm are advantageous under conditions of intense sperm competition. Nonetheless, previous work has been equivocal, perhaps because the intensity of sperm competition was measured indirectly. DNA profiling now provides a more direct measure of the number of offspring sired by extrapair males, and thus a more direct method of assessing the potential for sperm competition. Using a sample of 21 species of passerine birds for which DNA profiling data were available, we found a positive relation between sperm length and the degree of extrapair paternity. A path analysis, however, revealed that this relationship arises only indirectly through the positive relationship between the rate of extrapair paternity and length of sperm storage tubules (SSTs) in the female. As sperm length is correlated positively with SST length, an increase in the intensity of sperm competition leads to an increase in sperm length only through its effect on SST length. Why females vary SST length with the intensity of sperm competition is not clear, but one possibility is that it increases female control over how sperm are used in fertilization. Males, in turn, may respond on an evolutionary time scale to changes in SST size by increasing sperm length to prevent displacement from rival sperm. Previous theoretical analyses predicting that sperm size should decrease as sperm competition becomes more intense were not supported by our findings. We suggest that future models of sperm‐size evolution consider not only the role of sperm competition, but also how female control and manipulation of ejaculates after insemination selects for different sperm morphologies.

Sperm Size and Sperm Competition in Birds

In a sample of 20 species of North American passerine birds we found no relation between sperm size and mating system like that previously reported in mammals (Gomendio & Roldan (Proc. R. Soc. Lond. B 243, 181 (1991)). Instead, we found a positive correlation between sperm length and the length of female sperm storage tubules (SSTS) and a negative correlation between sperm length and the number of SSTS. Both of these correlations suggest that the more than fivefold variation in sperm size we found among species can be explained by sperm competition for access to storage sites (SSTS) in females. As longer sperm appear to be able to swim faster, selection should favour long sperm when SSTS are in short supply; sperm long enough to fill an SST might also prevent access to SSTS by the sperm of other males. Conversely, selection should favour shorter sperm when there is an advantage to sperm layering within an SST promoting a lastmale mating advantage. Although we conclude that sperm competition influences sperm size in birds, little is known about the interactions between sperm and SSTS. It seems clear, however, that detailed study of this interaction will provide a new dimension to the study of avian mating systems.

Female promiscuity promotes the evolution of faster sperm in cichlid fishes

Sperm competition, the contest among ejaculates from rival males to fertilize ova of a female, is a common and powerful evolutionary force influencing ejaculate traits. During competitive interactions between ejaculates, longer and faster spermatozoa are expected to have an edge; however, to date, there has been mixed support for this key prediction from sperm competition theory. Here, we use the spectacular radiation of cichlid fishes from Lake Tanganyika to examine sperm characteristics in 29 closely related species. We provide phylogenetically robust evidence that species experiencing greater levels of sperm competition have faster-swimming sperm. We also show that sperm competition selects for increases in the number, size, and longevity of spermatozoa in the ejaculate of a male, and, contrary to expectations from theory, we find no evidence of trade-offs among sperm traits in an interspecific analysis. Also, sperm swimming speed is positively correlated with sperm length among, but not within, species. These different responses to sperm competition at intra- and interspecific levels provide a simple, powerful explanation for equivocal results from previous studies. Using phylogenetic analyses, we also reconstructed the probable evolutionary route of trait evolution in this taxon, and show that, in response to increases in the magnitude of sperm competition, the evolution of sperm traits in this clade began with the evolution of faster (thus, more competitive) sperm.

Nestling American robins compete with siblings by begging

SummaryThe evolution of intense begging by dependent nestling birds has recently been the subject of several theoretical papers. The interesting problem here is that nestlings should be able to communicate their nutritional status to parents in ways that are less costly energetically and less likely to attract predators. Thus, conspicuous begging behaviour is thought to have evolved as a result of either competition among nestmates or the manipulation of their parents to provide more food than would otherwise be favoured by selection. We studied sibling competition for parental feedings in the American robin (Turdus migratorius). We demonstrate that the probability that an individual nestling received food was related to several indices of begging. When we experimentally prevented parents from feeding part of their brood, both the intensity of begging and the number of feedings subsequently received by food-deprived nestlings increased. Furthermore, the begging intensity of those nestlings that were not food-deprived also increased in response to the begging of their hungrier siblings.

Sperm swimming speed and energetics vary with sperm competition risk in bluegill (Lepomis macrochirus)

Under sperm competition, a male’s fertilization success depends largely on the ejaculate characteristics of competing males. Theoretical models predict that, in external fertilizers, increased risk of sperm competition should result in selection for increased sperm swimming speed. To test this prediction, we studied the behavior of sperm from parental and sneaker male bluegill (Lepomis macrochirus), a fish species characterized by high levels of cuckoldry due to alternative reproductive tactics of males (parentals and cuckolders). Because cuckolders (sneakers and satellites) always spawn in the presence of a parental male, but the reverse is not true, cuckolders experience the greater risk of sperm competition. We show here that the spermatozoa of sneakers have faster initial swimming speeds but shorter periods of motility than the sperm of parental males. Moreover, we show that sperm swimming speeds shortly after activation (when most fertilization occurs) are correlated with starting ATP levels in spermatozoa, suggesting that sperm competition has selected for higher energetic capacity in the sperm of sneakers. Thus, the higher energetic capacity and initial swimming speed of sneaker sperm may explain why, despite having fewer sperm per ejaculate than parentals, sneakers fertilize more eggs than parental males when they compete to fertilize a clutch of eggs.