Spatial and temporal escape from fungal parasitism in natural communities of anciently asexual bdelloid rotifers.

Sexual reproduction is costly, but it is nearly ubiquitous among plants and animals, whereas obligately asexual taxa are rare and almost always short-lived. The Red Queen hypothesis proposes that sex overcomes its costs by enabling organisms to keep pace with coevolving parasites and pathogens. If so, the few cases of stable long-term asexuality ought to be found in groups whose coevolutionary interactions with parasites are unusually weak. In theory, antagonistic coevolution will be attenuated if hosts disperse among patches within a metapopulation separately from parasites and more rapidly. We examined whether these conditions are met in natural communities of bdelloid rotifers, one of the longest-lived asexual lineages. At any life stage, these microscopic invertebrates can tolerate the complete desiccation of their ephemeral freshwater habitats, surviving as dormant propagules that are readily carried by the wind. In our field experiments, desiccation and wind transport enabled bdelloids to disperse independently of multiple fungal parasites, in both time and space. Surveys of bdelloid communities in unmanipulated moss patches confirmed that fungal parasitism was negatively correlated with extended drought and increasing height (exposure to wind). Bdelloid ecology therefore matches a key condition of models in which asexuals persist through spatio-temporal decoupling from coevolving enemies.

Why on earth?: Evaluating hypotheses about the physiological functions of human geophagy.

Geophagy has been hypothesized to be an adaptive behavior, either as a means to allay nutrient deficiency or to protect against ingested pathogens and toxins. Others have proposed that geophagy is non-adaptive, occurring either to allay hunger or as an epiphenomenon of nutrient deficiencies. This paper evaluates these hypotheses using 482 published cultural-level accounts of human geophagy and 330 accounts of geophagy among 297 species of mammals, birds, and reptiles. Information was extracted from reports of human geophagy to permit statistical analysis; reports of non-human geophagy were tabulated. Human geophagy did not parallel changes in nutrient requirements, occurred most frequently among children and pregnant women and in tropical areas (where pathogen densities are highest), and was associated with ingestion of toxic substances and gastrointestinal distress. Earth ingested by humans was craved and carefully selected and prepared; it had high clay content, but few bioavailable mineral nutrients. In primates, geophagy was associated with both protection from toxins and obtaining nutrients, whereas in other vertebrates it was associated mainly with obtaining nutrients. Our results indicate that human geophagy is best explained as providing protection from dietary chemicals, parasites, and pathogens, whereas animal geophagy may involve both micronutrient acquisition and protection.

Endangered species and a threatened discipline: behavioural ecology.

Behavioural ecologists often see little connection between the current conservation crisis and the future of their discipline. This view is myopic because our abilities to investigate and interpret the adaptive significance and evolutionary histories of behaviours are increasingly being compromised in human-dominated landscapes because of species extinctions, habitat destruction, invasive species, pollution, and climate change. In this review, we argue that many central issues in behavioural ecology will soon become prohibitively difficult to investigate and interpret, thus impeding the rapid progress that characterizes the field. To address these challenges, behavioural ecologists should design studies not only to answer basic scientific questions but also to provide ancillary information for protection and management of their study organisms and habitats, and then share their biological insights with the applied conservation community.

Anciently asexual bdelloid rotifers escape lethal fungal parasites by drying up and blowing away.

Asexuality has major theoretical advantages over sexual reproduction. An important evolutionary puzzle, therefore, is why exclusively asexual metazoan lineages rarely endure. The Red Queen hypothesis posits that asexuality is rapidly extinguished by relentlessly coevolving parasites and pathogens. If so, any long-lasting asexual lineage must have unusual alternative mechanisms to deal with these biotic enemies. Bdelloid rotifers are freshwater invertebrates that abandoned sexual reproduction millions of years ago. Here, we show that cultured populations of bdelloids can rid themselves of a deadly fungal parasite through complete desiccation (anhydrobiosis) and disperse by wind to establish new populations in its absence. In Red Queen models, spatiotemporal escape can decouple and protect asexuals from coevolving enemies. Thus, our results may help to explain the persistence of the anciently asexual Bdelloidea.

Morning sickness: adaptive cause or nonadaptive consequence of embryo viability?

"Morning sickness" is the common term for nausea and vomiting in early human pregnancy (NVP). Recent interest in why NVP occurs-that is, in the evolutionary costs and benefits of NVP-has spurred the development of two alternative hypotheses. The "prophylaxis," or "maternal and embryonic protection," hypothesis suggests that NVP serves a beneficial function by expelling foods that may contain harmful toxins and microorganisms and triggering aversions to such foods throughout pregnancy. The alternative "by-product" hypothesis suggests that NVP is a nonfunctional by-product of conflict--over resource allocation--between the pregnant woman and the embryo. The critical predictions of the prophylaxis hypothesis have been developed and tested, whereas the by-product hypothesis has not been subjected to similar scrutiny. To address this gap, we developed a graphical model and used it to derive predictions from the by-product hypothesis under two different assumptions, namely, that NVP is either (i) a by-product of current conflict between a pregnant woman and an embryo or (ii) a by-product of honest signals of viability produced by the embryo. Neither version of the by-product hypothesis is fully consistent with available data. By contrast, the timing of NVP, its variation among societies, and associated patterns of food cravings and aversions are consistent with the prophylaxis hypothesis.

Allergies: their role in cancer prevention.

The nature of the biological relationships between cancers and allergies has intrigued researchers and health care providers for five decades. Three hypotheses have been proposed: antigenic stimulation predicts positive associations between cancers and allergies (i.e., allergy sufferers are more likely to get cancer), whereas immunosurveillance and prophylaxis predict inverse associations (i.e., allergy sufferers are less likely to get cancer). Immunosurveillance predicts inverse associations for cancers of all tissues and organ systems, and prophylaxis predicts inverse associations specifically for cancers of tissues and organ systems that interface with the external environment. To comparatively evaluate these hypotheses, we comprehensively reviewed the literature on cancer and allergies. We located 148 papers published from 1955 through 2006 that reported results of 463 studies of relationships between patients' histories of 11 specific allergies and cancers of 19 tissues and organ systems, and 183 studies of patients' histories of multiple allergies in relation to various types/sites of cancers. Analyses of these studies revealed that (1) frequencies of positive, inverse, and null allergy-cancer associations differed considerably among cancers of different tissues and organ systems; (2) more than twice as many studies reported inverse allergy-cancer associations as reported positive associations; (3) inverse associations were particularly common for cancers of the mouth and throat, brain glia, colon and rectum, pancreas, skin, and cervix but (4) particularly rare for cancers of the breast, prostate, and brain meninges, and for myeloma, non-Hodgkin's lymphoma, and myelocytic leukemia; (5) lung cancer was positively associated with asthma but inversely associated with other allergies; (6) inverse associations with allergies were more than twice as common for cancers of nine tissues and organ systems that interface with the external environment compared to cancers of nine tissues and organ systems that do not interface with the external environment; and (7) eczema, hives, and allergies to animal dander and food were most frequently inversely associated with cancers of tissues that interface with the external environment. Taken together, these results are more consistent with the prophylaxis hypothesis than the two alternatives. IgE is a widespread and ancient immunoglobulin isotype in mammals, occurring among all known marsupials, monotremes, and eutherians. The IgE system and its associated allergy symptoms may serve a common protective function: the rapid expulsion of pathogens, dangerous natural toxins, and other carcinogenic antigens before they can trigger malignant neoplasia in exposed tissues.

Maximum longevities of chemically protected and non-protected fishes, reptiles, and amphibians support evolutionary hypotheses of aging.

Evolutionary hypotheses of aging predict that species with low rates of mortality from extrinsic sources, such as predation, should senesce more slowly and have longer maximum life spans than related species with higher rates of extrinsic mortality. We tested this prediction by synthesizing information on maximum body lengths and life spans in captivity of 1193 species of chemically protected (venomous or poisonous) and non-chemically protected fishes, snakes, caudatans (salamanders and newts), and anurans (frogs and toads). In every phylogenetic group maximum longevity was positively correlated with body size and, when size was controlled for statistically, chemically protected species and genera usually had longer maximum life spans than non-protected species. These results reemphasize the importance of life history traits, particularly protection from predation, in the evolution of senescence.

Reflections on animal selves.

Is self-cognizance a uniquely human attribute, or do other animals also have a sense of self? Although there is considerable interest in this question, answers remain elusive. Progress has been stymied by misunderstandings in terminology, a focus on a narrow range of species, and controversies over key concepts, experimental paradigms and interpretations of data. Here, we propose a new conceptual and terminological framework, emphasizing that degrees of self-cognizance differ among animals because of the cognitive demands that their species-specific social structures and life-history characteristics have placed upon them over evolutionary time. We suggest that the self-cognizance of an organism falls at a point on a continuum of social complexity and conscious involvement.

Nestling recognition via direct cues by parental male bluegill sunfish ( Lepomis macrochirus).

Parental care can be costly to a parent in terms of both time and energy invested in the young. In species with cuckoldry or brood parasitism not all of the young under a parent's care are necessarily offspring. In such cases, distinguishing between kin and non-kin, and investing only in the former (nepotism), can be advantageous. Bluegill sunfish ( Lepomis macrochirus) are characterized by paternal care and cuckoldry, and care-providing males appear to show nepotistic behaviours. Here, we investigated nestling recognition in bluegill, determining whether parental males can differentiate between young from their own nest (familiar and related) and young from non-neighbouring nests (unfamiliar and unrelated) using (1) visual and chemical cues, and (2) chemical cues only. In the first experiment, wild-caught parental males were presented with samples of eggs or fry (newly hatched eggs) collected from their own nest or a foreign nest and placed on opposite sides of an aquarium. The time these parental males spent associating with each sample, and their "pecking" behaviours (indicating cannibalism), were recorded. Parental males showed no preference between eggs from their own nest and eggs from a non-neighbouring nest, but they preferred to associate with fry from their own nest over foreign fry. There also was a positive relationship between male body size and the time spent associated with fry from their own nest. Parental males pecked at foreign fry more than 5 times as often as fry from their own nest, though this difference was not statistically significant. In the second experiment, fry that were collected from the nest of a wild-caught parental male or a non-neighbouring nest were placed in different containers and the water from each was dripped into opposite ends of an aquarium. The time the male spent on each side was recorded. In this case, parental males spent more time near the source of water conditioned by unrelated fry, but there was a positive relationship between male condition (fat reserves) and the time he spent near the source of water conditioned by fry from his own nest. Results confirm that chemicals cue nestling recognition by parental male bluegill.

Decision making and recognition mechanisms.

Determining how individuals adjust their behaviour to maximize reproductive opportunities is fundamental to understanding the adaptive significance of behavioural variations. Such 'decision making' requires recognition mechanisms, whereby an individual evaluates cues that yield information about the potential reproductive outcomes of alternative behaviours. Here, we develop a quantitative model for understanding how individuals evaluate cues. Only when a proximate (immediate) cue predicts reproductive value more reliably than an evolved predisposition, will the cue influence an individual's decision. The model resolves some long-standing controversies in evolutionary biology involving recognition mechanisms and interpretations of behavioural decisions that were observed after manipulations of cues of parentage, kinship and mate quality.

Nausea and vomiting of pregnancy in an evolutionary perspective.

The proximate mechanisms underlying gestational nausea and vomiting have been intensively studied, but the possibility that the symptoms themselves serve a useful function has only recently been considered seriously. We synthesized evidence to evaluate various hypotheses for the adaptive significance of nausea and vomiting of pregnancy, as well as the possibility that symptoms are nonfunctional byproducts of pregnancy hormones. We found greatest support for the hypothesis that normal levels of nausea and vomiting of pregnancy (excluding hyperemesis) protect pregnant women and their embryos from harmful substances in food, particularly pathogenic microorganisms in meat products and toxins in strong-tasting plants. We discuss the data that support critical predictions of this "maternal and embryo protection hypothesis" (and contradict other hypotheses), as well as appropriate implications of these results. Knowledge that normal nausea and vomiting of pregnancy indicates the functioning of a woman's defense system, rather than a bodily malfunction, may reassure patients and enable health care providers to develop new ways of minimizing the uncomfortable symptoms.