Michael P. Lombardo

Access to mutualistic endosymbiotic microbes: an underappreciated benefit of group living

A central question in behavioral ecology has been why animals live in groups. Previous theories about the evolution of sociality focused on the potential benefits of decreased risk of predation, increased foraging or feeding efficiency, and mutual aid in defending resources and/or rearing offspring. This paper argues that access to mutualistic endosymbiotic microbes is an underappreciated benefit of group living and sets out to reinvigorate Troyer’s hypothesis that the need to obtain cellulolytic microbes from conspecifics influenced the evolution of social behavior in herbivores and to extend it to nonherbivores. This extension is necessary because the benefits of endosymbionts are not limited to nutrition; endosymbionts also help protect their hosts from pathogens. When hosts must obtain endosymbionts from conspecifics, they are forced to interact. Thus, complex forms of sociality may be more likely to evolve when hosts must repeatedly obtain endosymbionts from conspecifics than when endosymbionts can be obtained either directly from the environment, are vertically transmitted, or when repeated inoculations are not necessary. Observations from a variety of taxa are consistent with the ideas that individuals benefit from group living by gaining access to endosymbionts and the complexity of social behavior is associated with the mode of acquisition of endosymbionts. Ways to test this theory include (a) experiments designed to examine the effects of endosymbionts on host fitness and how endosymbionts are obtained and (b) using phylogenetic analyses to examine endosymbiont–host coevolution with the goal of determining the relationship between the mode of endosymbiont acquisition and host sociality.

On the Evolution of Sport

Sports have received little attention from evolutionary biologists. I argue that sport began as a way for men to develop the skills needed in primitive hunting and warfare, then developed to act primarily as a lek where athletes display and male spectators evaluate the qualities of potential allies and rivals. This hypothesis predicts that (1) the most popular modern male sports require the skills needed for success in male-male physical competition and primitive hunting and warfare; (2) champion male athletes obtain high status and thereby reproductive opportunities in ways that parallel those gained by successful primitive hunters and warriors; (3) men pay closer attention than do women to male sports so they can evaluate potential allies and rivals; and (4) male sports became culturally more important when opportunities to evaluate potential allies and rivals declined as both the survival importance of hunting and the proportion of men who experience combat decreased. The characteristics of primitive and modern sports are more consistent with these predictions than those generated by intersexual sexual selection theories of sport.

Nest Architecture and Reproductive Performance in Tree Swallows (Tachycineta bicolor)

ABSTMACT.-Nests are an important component of parental effort in birds. From 1988 to 1990, I compared the architecture of nests built by subadult and adult female Tree Swallows (Tachycineta bicolor) in boxes in southeastern Michigan in order to determine if there were age-related differences in nest architecture and if these differences were associated with agerelated differences in reproductive performance. Nests built by Tree Swallows were composed of a mat of dry grasses and a nest cup lined with feathers. On average, nest material filled approximately 30% of a nest box. I observed few age-related differences in nest architecture. However, nests built by subadult females were significantly less well feathered than nests built by adult females, but feather score was not correlated with the production of nestlings or fledglings. There were age-related and within-season variations in reproductive performance associated with variations in nest architecture, especially later in the season. Among subadult females that bred later in the season (i.e. after the population median date of clutch initiation), those females that built larger nests (as indicated by total nest volume, depth of material beneath the nest cup, and percentage of nest box filled with material) hatched more eggs per clutch. In 1990, subadult females that bred later in the season and built larger nests (as indicated by depth of material beneath nest cup and percentage of nest box filled with material) produced significantly more hatchlings but significantly fewer fledglings. Among adult females that bred later in the season, those females that built nests that filled a larger percentage of the nest box hatched fewer eggs. Adult females with nests having larger cups produced significantly more fledglings, but those with cups crowded with nestlings (as indicated by a cup index [total egg volume/nest cup volume]) produced significantly fewer fledglings. In 1990, adult females that bred later in the season and built larger nests (as indicated by depth of nest material, total nest volume, percentage of nest box filled with material) and had more-crowded nest cups produced fewer hatchlings and fledged a significantly smaller proportion of hatchlings. These results suggest that nestling hyperthermia in well-insulated nests may affect the reproductive performance of Tree Swallows that breed late in the season. Received 11 January 1993, accepted 1 July 1993.

On the Evolution of Sexually Transmitted Diseases in Birds

Sexually transmitted diseases (STDs) in animals are caused by pathogens that are transmitted during copulation. Birds have played an important role in the development of STD-centered theories of mating behavior. However, it is not known whether STDs exist in wild bird populations. While the avian cloaca with its dual functions of gamete transfer and excretion seemingly predisposes birds for the evolution of STDs, the life history patterns of most birds (i.e., seasonal breeders with relatively brief annual periods of sexual activity) suggest otherwise. The importance of STDs as selective forces that shape host biology depends on whether host life history patterns provide the necessary conditions for the evolution and spread of virulent pathogens that rely on host copulation for dispersal. Infrequent dispersal opportunities for microbes that rely on host sexual contact for dispersal should favor the evolution of low pathogen virulence, persistent infection, and lengthened infectious periods. I examine the disease characteristics of documented STDs that are relevant to birds in order to evaluate the (1) importance of STDs as selective forces in birds and (2) ecological conditions in which avian STDs are likely to be discovered. I conclude that socially monogamous short-lived birds with short breeding cycles and altricial nestlings (e.g., temperate zone songbirds) are not likely to have coevolved with highly virulent STDs which would be important selective forces. However, virulent STDs may have evolved in birds with one or more of the following life history characteristics: long life spans, long breeding cycles, multiple matings, and precocial young because these conditions produce increased opportunities for pathogen transmission and can favor the evolution of virulence. These life history characteristics are found and exaggerated in the birds for which STDs have been documented, the domesticated fowl and waterfowl.

Spatiotemporal Patterns in Nest Box Occupancy by Tree Swallows Across North America

Data from the North American Breeding Bird Survey (BBS) suggest that populations of aerial insectivorous birds are declining, particularly in northeastern regions of the continent, and particularly since the mid-1980s. Species that use nest boxes, such as Tree Swallows (Tachycineta bicolor), may provide researchers with large data sets that better reveal finer-scale geographical patterns in population trends. We analyzed trends in occupancy rates for ca. 40,000 Tree Swallow nest-box-years from 16 sites across North America. The earliest site has been studied intensively since 1969 and the latest site since 2004. Nest box occupancy rates declined significantly at five of six (83%) sites east of -78° W longitude, whereas occupancy rates increased significantly at four of ten sites (40%) west of -78° W longitude. Decreasing box occupancy trends from the northeast were broadly consistent with aspects of a previous analysis of BBS data for Tree Swallows, but our finding of instances of increases in other parts of the continent are novel. Several questions remain, particularly with respect to causes of these broadscale geographic changes in population densities of Tree Swallows. The broad geographic patterns are consistent with a hypothesis of widespread changes in climate on wintering, migratory, or breeding areas that in turn may differentially affect populations of aerial insects, but other explanations are possible. It is also unclear whether these changes in occupancy rates reflect an increase or decrease in overall populations of Tree Swallows. Regardless, important conservation steps will be to unravel causes of changing populations of aerial insectivores in North America. RESUME. Les donnees provenant du Releve des oiseaux nicheurs (BBS) de l’Amerique du Nord semblent indiquer que les populations d’insectivores aeriens sont en declin, particulierement dans les regions du nord-est du continent et depuis le milieu des annees 1980. Grâce aux especes qui utilisent les nichoirs, comme l’Hirondelle bicolore (Tachycineta bicolor), les chercheurs ont acces a une grande quantite de donnees qui revelent davantage les tendances des populations a l’echelle fine. Nous avons analyse la tendance du taux d’occupation par l’Hirondelle bicolore a partir de 40 000 nichoirs-annees provenant de 16 sites repartis en Amerique du Nord. Le site le plus ancien est suivi intensivement depuis 1969 et le plus recent, depuis 2004. Le taux d’occupation des nichoirs a diminue significativement dans 5 des 6 sites (83 %) situes a l’est du 78° de longitude ouest, tandis qu’il a augmente significativement dans 4 des 10 sites (40 %) a l’ouest du 78° de longitude ouest. La tendance a la baisse de l’occupation observee dans le nord-est concorde dans les grandes lignes avec les resultats d’une analyse anterieure des donnees du BBS pour cette espece, mais les hausses que nous avons observees dans d’autres regions de l’Amerique du Nord s’averent nouvelles. Plusieurs interrogations demeurent, notamment en ce qui a trait aux causes de ces changements dans la densite des populations d’Hirondelles bicolores a grande echelle. Ces vastes tendances geographiques concordent avec l’hypothese de changements climatiques generalises qui toucheraient les aires d’hivernage, de migration ou de nidification, lesquels pourraient affecter differemment les populations d’insectes aeriens, mais d’autres explications sont aussi possibles. En outre, nous ne savons pas si ces changements du taux d’occupation refletent une hausse ou une baisse dans l’ensemble des populations d’Hirondelles bicolores. Neanmoins, pour assurer leur conservation, il sera important d’elucider les causes des changements de populations chez les insectivores aeriens en Amerique du Nord.

Digit Ratios in Green Anolis Lizards (Anolis carolinensis)

The development of tetrapod digits is directed by the Homeobox (Hox) genes. The expression of Hox genes is influenced by exposure to endogenous sex steroids during development so that prenatal exposure to estrogens and androgens positively influences the lengths of digits 2 (2D) and 4 (4D), respectively. Because of this, Manning ( 2002 ) predicted that male tetrapods should have smaller 2D:4D than that of females because males are exposed to higher levels of androgens during development. We measured digits in green anolis lizards (Anolis carolinensis) to (a) test Mannings prediction; (b) compare our results with those of other studies of digit ratios in reptiles and birds to test the phylogenetic constraint hypothesis, which argues that the digit ratios of reptiles and birds should be more similar to each other than either taxa is to mammals because the patterns have been conserved in living diapsids; and (c) compare our results with those of another study of digit ratio in anoles (Chang et al., 2006 ). We did not detect evidence of sexual dimorphism in 2D:4D. Our results did not support either Mannings prediction or the phylogenetic constraint hypothesis. Furthermore, our results did not match those found in Chang et al. ( 2006 ), suggesting that digit ratios in anolis lizards may not be reliable indicators of prenatal exposure to hormones. Anat Rec, 291:433–440, 2008.

Innate Immune Response Development in Nestling Tree Swallows

Abstract We tracked the development of innate immunity in nestling Tree Swallows (Tachycineta bicolor) and compared it to that of adults using blood drawn from nestlings during days 6, 12, and 18 of the ∼20-day nestling period and from adults. Innate immunity was characterized using an in vitro assay of the ability of whole blood to kill Escherichia coli. The ability of whole blood to kill E. coli increased as nestlings matured. Neither this component of innate immunity nor right wing chord length on day18 were as developed as in adults indicating that development of the innate immune system and growth both continued after fledging. Narrow sense heritability analyses suggest that females with strong immune responses produced nestlings with strong immune responses. These data suggest nestling Tree Swallows allocated sufficient energy to support rapid growth to enable fledging by day 18, but that further development of innate immunity occurred post-fledging.

A possible case of adult intraspecific killing in the tree swallow

Despite considerable interest in its occurrence or potential occurrence (e.g., Lorenz 1963), both direct and circumstantial evidence of intraspecific killing in adult passerines is rare (see Davis 1940, Cottrille 1950, Grubbs 1977, Loflin 1982). The purpose of this note is to add to this meager data base by presenting evidence of intraspecific killing in adult Tree Swallows (Tachycineta bicolor). My study site is a nest box colony on the salt marshes of the John F. Kennedy Memorial Wildlife Refuge located adjacent to Tobay Beach on the south shore of Long Island, New York (see Schaeffer 1972 for a description of the study site). On 10 Mav 1983 I discovered two birds. a male and a female in brown second-year plumage (see Dwight 1900, Cohen 1980, Hussell 1983) inside Box 134 during a routine census. The male was on top of the female. I banded both birds with U.S. Fish & Wildlife Service aluminum bands. The box did not contain nesting material. I returned to Box 134 on 14 May 1983 and found the female dead on the floor of the box, flat on her stomach with her wings spread out to her sides. Her head was tilted up and back; her forehead was defeathered and covered with dried blood and puncture wounds. For several reasons, I believe that another Tree Swallow caused these wounds. First, no other species used the nest boxes at my study site. Therefore, Tree Swallows competed only among themselves for these sites, so it is unlikely that an interspecific nest site competitor was responsible for the female’s death. Second, Kuerzi (194 1) presented evidence of intraspecific killing in Tree Swallows and reported two fights between a male and a female in brown plumage. During one fight the brown female had the male pinned on the ground, and she pecked at the back of his head until he escaped when Kuerzi approached for a better view. Kuerzi (1941) also reported that a Tree Swallow killed a female Eastern Bluebird (Sialia siulis). This evidence indicates that Tree Swallows are capable of inflicting mortal wounds on one another. Third, infanticide is known in this species (Shelley 1934). Quinney (1983) attributed the greater disappearance rate of eggs and very young nestlings at polygynous nests relative to monogamous nests to the action of females attempting to prevent other females from using the same nest box in polygynous pairs. In 198 1 I found a dead one-day-old nestling with a puncture wound behind one eye, a type of wound common in victims of avian infanticide (see Mock 1984; Crook and Shields, 1985). Last, in an experiment to determine the

Nestling Tree Swallow (Tachycineta bicolor) Diets in an Upland Old Field in Western Michigan

Abstract We collected and identified 1852 prey items from 89 boluses delivered to 62 nestling tree swallows (Tachycineta bicolor) at 14 nests in an upland old field in western Michigan. We found that 90.8% of nestling diets was insects from the Orders Diptera, Homoptera, Hymenoptera and Coleoptera. We also found clam and snail shells in boluses. Over the most common brood sizes of 4–6 nestlings, brood size was inversely proportional to the number of items per bolus delivered to nestlings although mean dry and mean organic weight of boluses did not differ. Bolus composition was not influenced by weather conditions. Nestling diets at our study site were similar in the proportions of many prey items, such as Diptera and Homoptera, to tree swallow nestling diets in other habitats but contained fewer aquatic forms such as Odonata and Ephemeroptera.

Digit Ratio in Birds

The Homeobox (Hox) genes direct the development of tetrapod digits. The expression of Hox genes may be influenced by endogenous sex steroids during development. Manning (Digit ratio. New Brunswick, NJ: Rutgers University Press, 2002) predicted that the ratio between the lengths of digits 2 (2D) and 4 (4D) should be sexually dimorphic because prenatal exposure to estrogens and androgens positively influence the lengths of 2D and 4D, respectively. We measured digits and other morphological traits of birds from three orders (Passeriformes, house sparrow, Passer domesticus; tree swallow, Tachycineta bicolor; Pscittaciformes, budgerigar, Melopsittacus undulates; Galliformes, chicken, Gallus domesticus) to test this prediction. None were sexually dimorphic for 2D:4D and there were no associations between 2D:4D and other sexually dimorphic traits. When we pooled data from all four species after we averaged right and left side digits from each individual and z‐transformed the resulting digit ratios, we found that males had significantly larger 2D:4D than did females. Tetrapods appear to be sexually dimorphic for 2D:4D with 2D:4D larger in males as in some birds and reptiles and 2D:4D smaller in males as in some mammals. The differences between the reptile and mammal lineages in the directionality of 2D:4D may be related to the differences between them in chromosomal sex determination. We suggest that (a) natural selection for a perching foot in the first birds may have overridden the effects of hormones on the development of digit ratio in this group of vertebrates and (b) caution be used in making inferences about prenatal exposure to hormones and digit ratio in birds. Anat Rec, 2008.