Paul W. Sherman

Density and extra-pair fertilizations in birds: a comparative analysis

Abstract Møller and Birkhead (1992, 1993) reported that extra-pair copulations (EPCs) occur more frequently in colonial than dispersed nesting birds. We comprehensively reviewed published data to investigate how breeding density affects extra-pair fertilizations (EPFs). Within species EPFs appeared to increase with density: two of three studies on colonial breeders and six of eight on dispersed nesters showed increases in EPFs with increasing density. However, comparisons among species (n = 72) revealed no evidence that EPF frequencies correlated with (1) nesting dispersion, (2) local breeding density, or (3) breeding synchrony, even when each of these variables in turn was held constant and phylogenetic relationships were taken into account via contrast analyses. Methodological and biological reasons for the disparity between observational studies of EPCs and molecular genetic analyses of EPFs are discussed.

Mammalian eusociality: a family affair

Comparative studies of two species of mole-rat are helping to clarify the ecological correlates of mammalian eusociality. Both species live in social groups composed of close kin, within which breeding is restricted to one female and one to three males. They inhabit xeric areas with dispersed, patchy food and unpredictable rainfall. During droughts, they can neither expand their tunnel systems nor disperse. In brief periods after rain the animals must cooperate and dig furiously to locate rich food patches. By living in groups, arid-zone mole-rats can take full advantage of windows of opportunity when conditions are right for burrowing. Thus, ecological factors and kin selection have apparently interacted in the evolution of eusociality in these species.

Parasites, Pathogens, and Polyandry in Social Hymenoptera

Multiple mating by females with different males is widespread among insects, both solitary and social species (reviews in Walker 1980; Page and Metcalf 1982; Cole 1983; Starr 1984). Such polyandry creates opportunities for sperm competition (Parker 1984), a frequent outcome of which is multiple paternity within broods (e.g., in wasps, Metcalf and Whitt 1977, Muralidharan etal. 1986, Ross 1986; in ants, Pamilo 1982). Because multiple mating can thus reduce the average genetic relationship among female nest mates, polyandry represents an intriguing paradox for the original kin-selection explanations for the evolution of hymenopteran eusociality (Hamilton 1964, 1972; Starr 1979). Moreover, mating multiply may expose queens to increased chances of being preyed on or of contracting venereal diseases. Not surprisingly, therefore, considerable interest has recently been focused on the causes and consequences of multiple mating in insects generally (Thornhill and Alcock 1983, pp. 449-471) and social insects particularly (Page 1980, 1986). In one extreme but well-documented case, honeybee queens (Apis mellifera) may mate 17 or more times (Adams et al. 1977). Because the sperm from different males mix extensively rather than clumping separately, workers from many patrilines are simultaneously present in each colony (data in Taber 1955; Kerr et al. 1980; Laidlaw and Page 1984). Evidence is rapidly accumulating that worker honeybees can distinguish between closely and distantly related larvae (Page and Erickson 1984; Visscher 1986) and between fulland half-sibling adults (Getz and Smith 1983), using learned cues of genetic origin (Breed et al. 1985; Getz and Smith 1986). In the hive, such discrimination is manifested as nepotism and differential aggression: workers rear, feed, and groom a disproportionately large number of their full sisters (in colonies with or without queens; Noonan 1986; Frumhoff and Schneider 1987) and attack and bite an inordinate proportion of half sisters (in queenless colonies; Evers and Seeley 1986). It seems likely that such discrimination among patrilines may sometimes compromise colony-level efficiency and thus the queens reproductive output. Regardless, evidence of intra-nest kin-recognition mechanisms implies a long evolutionary history of discrepant reproductive interests among colony members resulting from multiple mating. In view of the potential disadvantages stemming from polyandry and the fact

Self-referent phenotype matching: theoretical considerations and empirical evidence

In most birds and mammals, young are raised in family groups. The phenotypes of nestmates and parents are thus reliable cues for recognition of conspecifics and kin. However, in some species, young develop alone, or in broods of mixed relatedness (e.g. because of multiple paternity or maternity), or among heterospecifics or unrelated conspecifics (brood parasites). Under these circumstances, the best referent (model) for discriminating close from distant kin and heterospecifics from conspecifics might be ones own self. This recognition process is known as self-referent phenotype matching. Here we review recent experimental evidence of self-referencing and suggest that behavioral neuroscience can provide new tools and insights into how it works (its proximate mechanistic and ontogenetic bases) and why it exists (its adaptive significance).

Is avian humoral immunocompetence suppressed by testosterone

Abstract A key issue in sexual selection theory is how a correlation between male secondary sexual characters and male genetic quality can be maintained. The immunocompetence-handicap hypothesis proposes that testosterone-dependent male characters remain honest signals because of the immunosuppressive effect of elevated steroid hormone levels. The hypothesis requires that physiological levels of testosterone depress immune system function. We quantified testosterone titers and humoral immunocompetence of captive male and female red-winged blackbirds (Agelaius phoeniceus) at three points in the annual cycle (autumn, prebreeding, and breeding). We also conducted an implant experiment on the males to assess the effects of prolonged, above-normal testosterone titers on humoral immune responses. Humoral immunocompetence was measured as secondary antibody production to a non-pathogenic protein antigen, keyhole limpet hemocyanin, using an enzyme-linked immunosorbent assay we developed for A. phoeniceus. Secondary antibody responses of individuals were highly repeatable between sampling periods. Neither physiological nor above-normal levels of plasma testosterone suppressed secondary antibody production. In paired tests of the same individuals between prebreeding and breeding, and between breeding and implant, plasma testosterone increased significantly but secondary antibody responses were unaffected. We are confident in these results because with 80% power, an 11–14% difference in antibody titers would have been detected. There was no relationship between plasma testosterone levels and humoral immunocompetence in free-ranging males tested at the peak of breeding. These results cast doubt on a key assumption of the immunocompetence-handicap hypothesis.

Morning Sickness: A Mechanism for Protecting Mother and Embryo

Approximately two-thirds of women experience nausea or vomiting during the first trimester of pregnancy. These symptoms are commonly known as morning sickness. Hook (1976) and Profet (1988) hypothesized that morning sickness protects the embryo by causing pregnant women to physically expel and subsequently avoid foods that contain teratogenic and abortifacient chemicals, especially toxic chemicals in strong-tasting vegetables, caffeinated beverages and alcohol. We examined this hypothesis by comprehensively reviewing the relevant medical, psychological and anthropological literature. In its support, (i) symptoms peak when embryonic organogenesis is most susceptible to chemical disruption (weeks 6-18), (ii) women who experience morning sickness are significantly less likely to miscarry than women who do not (9 of 9 studies), (iii) women who vomit suffer fewer miscarriages than those who experience nausea alone, and (iv) many pregnant women have aversions to alcoholic and nonalcoholic (mostly caffeinated) beverages and strong-tasting vegetables, especially during the first trimester. Surprisingly, however, the greatest aversions are to meats, fish, poultry, and eggs. A cross-cultural analysis using the Human Relations Area Files revealed 20 traditional societies in which morning sickness has been observed and seven in which it has never been observed. The latter were significantly less likely to have animal products as dietary staples and significantly more likely to have only plants (primarily corn) as staples than the 20 societies in which morning sickness occurred. Animal products may be dangerous to pregnant women and their embryos because they often contain parasites and pathogens, especially when stored at room temperatures in warm climates. Avoiding foodborne microorganisms is particularly important to pregnant women because they are immunosuppressed, presumably to reduce the chances of rejecting tissues of their own offspring (Haig 1993). As a result, pregnant women are more vulnerable to serious, often deadly infections. We hypothesize that morning sickness causes women to avoid foods that might be dangerous to themselves or their embryos, especially foods that, prior to widespread refrigeration, were likely to be heavily laden with microorganisms and their toxins. The alternative hypotheses that morning sickness is (i) an epiphenomenon of mother-offspring genetic conflict or hormones associated with viable pregnancies, or (ii) an indicator to potential sexual partners and kin that the woman is pregnant, resulting in reduced sexual behavior and increased nepotistic aid, were not well supported. Available data are most consistent with the hypothesis that morning sickness serves an adaptive, prophylactic function.

Antimicrobial functions of spices: why some like it hot.

Although spices have been important for centuries in food preparation throughout the world, patterns of spice use differ considerably among cultures and countries. What factors underlie these differences? Why are spices used at all? to investigate these questions, we quantified the frequency of use of 43 spices in the meat-based cuisines of the 36 countries for which we could locate traditional cookbooks. A total 4578 recipes from 93 cookbooks was analysed. We also compiled information on the temperature and precipitation in each country, the ranges of spice plants, and the antibacterial properties of each spice. These data were used to investigate the hypothesis that spices inhibit or kill food-spoilage microorganisms. In support of this is the fact that spice plant secondary compounds are powerful antimicrobial (i.e., antibacterial and antifungal) agents. As mean annual temperatures (an indicator of relative spoilage rates of unrefrigerated foods) increased, the proportion of recipes containing spices, number of spices per recipe, total number of spices used, and use of the most potent antibacterial spices all increased, both within and among countries. Likewise, the estimated fraction of bacterial species inhibited per recipe in each country was positively correlated with annual temperature. Several alternative hypotheses were considered-that spices provide macronutrients, disguise the taste and smell of spoiled foods, or increase perspiration and thus evaporative cooling; it also is conceivable that spice use provides no benefits. However, none of these four alternatives was well supported by our data. The proximate reason spices are used obviously is to enhance food palatability. But the ultimate reason is most likely that spices help cleanse foods of pathogens and thereby contribute to the health, longevity and reproductive success of people who find their flavors enjoyable.

Problems of kin recognition

Behavioural ecologists have long assumed that animals discriminate between their kin and non-kin, but paid little attention to how animals recognize their relatives. Although the first papers on kin recognition mechanisms appeared barely 10 years ago, studies now appear frequently in journals of animal behaviour. Initial findings reveal that kin recognition abilities are surprisingly well-distributed throughout the animal kingdom. Yet an understanding of the evolutionary and ecological significance of these abilities demands further analyses of the components of kin recognition mechanisms and the social contexts in which they are expressed. Many controversies and unresolved issues remain, and experimental approaches to these problems promise to continue making kin recognition an important, rapidly moving discipline within behavioural ecology.

Extra-pair fertilizations in mountain white-crowned sparrows

SummaryA population of white-crowned sparrows (Zonotrichia leucophrys oriantha) located near Tioga Pass, in the central Sierra Nevada of California, was studied during the 1985 and 1986 breeding seasons to determine how often chicks were not the offspring of both adults who reared them. Blood samples were obtained from 35 nesting pairs and feather pulp specimens were collected from all 110 young they fledged. Electrophoretic analyses of 4 polymorphic loci revealed that a minimum of 9 nests (26%) contained a chick that could not have been conceived in a mating between the attending pair, and that at least 15 chicks (14%) were not offspring of both attending adults. Using two recently developed probability indices, it was estimated that 34%–38% of chicks hatched at the study site were not offspring of one of their putative parents. Because there was no evidence that intraspecific brood parasitism occurred, all the mismatched young apparently resulted from extrapair copulations. Our data, along with similar results from other species, raise new questions about sexual selection and patterns of parental care in monogamous birds.

Phylogeny and Evolutionary History of the Ground Squirrels (Rodentia: Marmotinae)

Although ground squirrels (Spermophilus) and prairie dogs (Cynomys) are among the most intensively studied groups of mammals with respect to their ecology and behavior, a well-resolved phylogeny has not been available to provide a framework for comparative and historical analyses. We used complete mitochondrial cytochrome b sequences to construct a phylogeny that includes all 43 currently recognized species in the two genera, as well as representatives of two closely related genera (Marmota and Ammospermophilus). In addition, divergence times for ground squirrel lineages were estimated using Bayesian techniques that do not assume a molecular clock. All methods of phylogenetic analysis recovered the same major clades, and showed the genus Spermophilus to be paraphyletic with respect to both Marmota and Cynomys. Not only is the phylogeny at odds with previous hypotheses of ground squirrel relationships, but it suggests that convergence in morphology has been a common theme in ground squirrel evolution. A well-supported basal clade, including Ammospermophilus and two species in the subgenus Otospermophilus, diverged from all other ground squirrels an estimated 17.5 million years ago. Between 10 and 14 million years ago, a relatively rapid diversification gave rise to lineages leading to marmots and to several distinct groups of ground squirrels. The Eurasian ground squirrels diverged from their North American relatives during this period, far earlier than previously hypothesized. This period of diversification corresponded to warming climate and spread of grasslands in western North America and Eurasia. Close geographic proximity of related forms suggests that most species evolved in or near their current ranges.