James V. Briskie

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.

Extra-pair paternity, sperm competition and the evolution of testis size in birds

Sperm competition should select for increased sperm production if the probability of fertilization by a specific male is proportional to the relative number of sperm inseminated. A review of the literature generally supports the predicted positive association between sperm production or allocation and various measures of the presumed intensity of sperm competition. However, it is not clear how increased sperm competition is related to extra-pair paternity, and it remains unknown whether certainty of paternity should be associated with relative testis size. Based on a large sample of bird species with information on extra-pair paternity gathered from the literature, we demonstrate that testis mass is related positively to the level of extra-pair paternity, after controlling for body size and phylogeny. Although large testes may be necessary to avoid sperm depletion in species in which males frequently engage in multi-pair copulations, we argue that selection has favoured increased testis mass in situations of more intense sperm competition in order to retaliate against copulations by rival males. The fact the males are not always successful in retaliating against rival ejaculates further suggests that females may largely control the allocation of paternity in birds and that increased sperm production by males may simply be a male strategy to make the best of a bad situation.

Begging intensity of nestling birds varies with sibling relatedness

Begging for food is one of the most conspicuous behaviours performed by nestling birds. Recent models suggest that the form and intensity of begging evolved not only to communicate nutritional requirements to parents but also as a mechanism for competing against siblings to obtain a greater share of parental resources. In an interspecific comparison of passerine birds, we show that the loudness of nestling begging calls increases as the relatedness amongst the members of a brood declines. Species with high levels of mixed parentage, as well as the brood-parasitic brown-headed cowbird (Molothrus ater), begged louder than their closest monogamous and non-parasitic relatives. These results support the hypothesis that sibling relatedness influences begging behaviour in birds, and suggests that increased intensity of begging can evolve whenever female promiscuity or brood parasitism lowers the coefficient of relatedness among nestmates.

NEST PREDATION AND THE EVOLUTION OF NESTLING BEGGING CALLS

Begging by nestling birds can be conspicuous and loud. Such displays are thought to function in signalling nestling condition and securing parental care, but they also may inadvertently attract the attention of predators. We compared the structure of nestling begging calls to the risk of predation among 24 species of birds breeding in a forest community in central Arizona. After controlling for body size and phylogeny, we found that species subject to greater nest predation had calls with higher frequency (pitch) and lower amplitude (loudness) than species subject to lower rates of nest predation. As these acoustic features make it difficult for potential predators to pinpoint the source of a sound, our results suggest that an increased risk of predation has led to the evolution of begging calls that minimize locatability. The relationship between call structure and the risk of predation also supports the hypothesis that attracting predators is a direct cost of begging and that such costs can constrain any evolutionary escalation in the intensity of nestling begging.

Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations

The brown‐headed cowbird (Molothrus ater) is a widespread, obligate brood parasite of North American passerine birds. In southern Manitoba, where hosts are sympatric with cowbirds, American robins (Turdus migratorius) ejected parasitic eggs from all experimentally parasitized clutches (N = 25) and no eggs were accepted for more than four days. In contrast, robins in northern Manitoba, an area where cowbirds do not breed, accepted parasitic eggs in 33% of nests (N = 18) for at least five days. Acceptance of experimental cowbird eggs by a second host, the yellow warbler (Dendroica petechia), was similar in allopatric (100% of 20 nests) and sympatric (88.6% of 35 nests) populations, but models of a female cowbird elicited greater nest defense by warblers in the area of sympatry. Neither host rejected eggs of conspecifics, thus, rejection of cowbird eggs was not an epiphenomenon of conspecific brood parasitism. These results support the hypothesis that recognition of cowbirds and their eggs evolved as adaptations to counter cowbird parasitism and not some other selection pressure. The expression of anti‐parasite defenses by some individuals within allopatric populations further suggests these traits may be controlled genetically but persist in such areas either through the continued introgression of rejecter genes from sympatric populations or because of the low cost of rejection behavior when parasitism is absent or rare.

Predation on Dependent Offspring

Predation on dependent offspring (i.e., offspring that depend on parents for care) forms a critical source of natural selection that may shape a diversity of life history traits. Selection from predation risk on dependent offspring can influence life history strategies of both offspring and parents. Such selection may act on both the form of plastic responses (e.g., the shape of norms of reaction) and mean expression of traits. Consideration of both levels of responses is key to understanding the ecological and evolutionary role of predation on dependent offspring. Here, we discuss how plastic responses and mean expression of life history traits may respond to selection from predation on dependent offspring in nests of birds (i.e., nest predation). We then review the expected effects and evidence for a diversity of life history traits, including clutch size, egg size, renesting rates, onset of incubation, parental incubation behavior, development rates and period lengths, parental feeding behavior, nestling begging, and nest conspicuousness. The evidence demonstrates a broad role of nest predation on both phenotypic plasticity and mean expression of diverse traits, but evidence remains limited to a few studies on a limited variety of species for almost all traits, and much broader experimental tests are needed.

Male sperm reserves and copulation frequency in birds

SummaryMale passerine birds store sperm in a cloacal protuberance during the breeding season. We consider three hypotheses to explain interspecific variation in relative cloacal protuberance size. The copulation efficiency hypothesis states that a relatively large cloacal protuberance facilitates sperm transfer and predicts more rapid copulation in species with larger protuberances. There is insufficient data to test this idea rigorously, but we found no evidence for such an effect. The spermatozoa size hypothesis is a non-functional hypothesis which states that cloacal protuberance size is merely a consequence of sperm size, and predicts that species with larger spermatozoa have relatively larger cloacal protuberances. Sperm length was positively correlated with protuberance size, providing support for this hypothesis, although it seems unlikely that variation in sperm size alone is sufficient to account for variation in protuberance size because the numbers of sperm stored in the cloacal protuberance were also positively correlated with its size. The sperm competition hypothesis states that the cloacal protuberance is a sperm store and predicts that when sperm competition is intense, as measured by male copulation frequency and or mating system, males will have relatively large protuberances and testes mass. The sperm competition hypothesis was supported: in a comparative study in which we controlled for phylogenetic effects, relative cloacal protuberance size was significantly and positively correlated with copulation frequency. Across all mating systems protuberance size was also positively correlated with the mass of seminal glomera tissue, the number of sperm stored in the seminal glomera, and with relative testes size. These results suggest that where sperm competition is intense, a large cloacal protuberance is required to maintain a large sperm reserve for a high copulation rate.

Patterns of sperm storage in relation to sperm competition in passerine birds

Using a technique for observing sperm storage tubules (SSTs) in whole-mount preparations of oviduct tissue, we estimated the number and length of SSTs across 20 species of passerine birds in seven subfamilies. The average number of SSTs per female varied ninefold across the species examined and was correlated positively with body mass and relative egg size, suggesting that much of the interspecific variation in the number of SSTs may be a consequence of allometry. However, after controlling for body mass, the number of SSTs per female was also negatively correlated with the average length of SSTs and we suggest this pattern could result from selection for greater sperm length when access to sperm storage sites is limited by females. SST length varied eight-fold across the species examined but unlike the number of SSTs, SST length was not correlated with body mass. Instead, SST length was strongly and positively correlated with sperm length, suggesting a history of coevolution between male gametes and sperm storage sites in females that is independent of body size. Neither mating system nor any of four other morphological variables (testis length, oviduct length, clutch size, sperm storage capacity) was consistently correlated with either the number or size of SSTs. Variation between species in the potential for sperm layering within an SST, however, indicates that the pattern of sperm precedence (i.e., the pattern of paternity relative to mating order) may vary from species to species. We propose that a conflict of interest between the sexes with respect to sperm storage could lead to an arms race between sperm length and SST length and may help explain both the diversity in sperm storage patterns among species and the influence of sperm storage on the evolution of mating behavior in birds.

Introduced mammalian predators induce behavioural changes in parental care in an endemic New Zealand bird.

The introduction of predatory mammals to oceanic islands has led to the extinction of many endemic birds. Although introduced predators should favour changes that reduce predation risk in surviving bird species, the ability of island birds to respond to such novel changes remains unstudied. We tested whether novel predation risk imposed by introduced mammalian predators has altered the parental behaviour of the endemic New Zealand bellbird (Anthornis melanura). We examined parental behaviour of bellbirds at three woodland sites in New Zealand that differed in predation risk: 1) a mainland site with exotic predators present (high predation risk), 2) a mainland site with exotic predators experimentally removed (low risk recently) and, 3) an off-shore island where exotic predators were never introduced (low risk always). We also compared parental behaviour of bellbirds with two closely related Tasmanian honeyeaters (Phylidonyris spp.) that evolved with native nest predators (high risk always). Increased nest predation risk has been postulated to favour reduced parental activity, and we tested whether island bellbirds responded to variation in predation risk. We found that females spent more time on the nest per incubating bout with increased risk of predation, a strategy that minimised activity at the nest during incubation. Parental activity during the nestling period, measured as number of feeding visits/hr, also decreased with increasing nest predation risk across sites, and was lowest among the honeyeaters in Tasmania that evolved with native predators. These results demonstrate that some island birds are able to respond to increased risk of predation by novel predators in ways that appear adaptive. We suggest that conservation efforts may be more effective if they take advantage of the ability of island birds to respond to novel predators, especially when the elimination of exotic predators is not possible.