Showing papers in "The Quarterly Review of Biology in 2001"

Mammalian Play: Training for the Unexpected

Abstract: In this review, we present a new conceptual framework for the study of play behavior, a hitherto puzzling array of seemingly purposeless and unrelated behavioral elements that are recognizable as play throughout the mammalian lineage. Our major new functional hypothesis is that play enables animals to develop flexible kinematic and emotional responses to unexpected events in which they experience a sudden loss of control. Specifically, we propose that play functions to increase the versatility of movements used to recover from sudden shocks such as loss of balance and falling over, and to enhance the ability of animals to cope emotionally with unexpected stressful situations. To obtain this "training for the unexpected," we suggest that animals actively seek and create unexpected situations in play through self-handicapping; that is, deliberately relaxing control over their movements or actively putting themselves into disadvantageous positions and situations. Thus, play is comprised of sequences in which the players switch rapidly between well-controlled movements similar to those used in "serious" behavior and self-handicapping movements that result in temporary loss of control. We propose that this playful switching between in-control and out-of-control elements is cognitively demanding, setting phylogenetic and ontogenetic constraints on play, and is underlain by neuroendocrinological responses that produce a complex emotional state known as "having fun." Furthermore, we propose that play is often prompted by relatively novel or unpredictable stimuli, and is thus related to, although distinct from, exploration. We present 24 predictions that arise from our new theoretical framework, examining the extent to which they are supported by the existing empirical evidence and contrasting them with the predictions of four major alternative hypotheses about play. We argue that our "training for the unexpected" hypothesis can account for some previously puzzling kinematic, structural, motivational, emotional, cognitive, social, ontogenetic, and phylogenetic aspects of play. It may also account for a diversity of individual methods for coping with unexpected misfortunes.

Sexually selected traits and adult survival: a meta-analysis.

Abstract: Traits correlated with male mating success are likely to be subject to sexual selection. Sexually selected characters are thought to be costly to develop and maintain. If males do not vary their investment in sexual traits in relation to their ability to bear the costs, there should be a negative relationship between male longevity or survival and the expression of sexual traits. In particular, a negative relationship is predicted by pure Fisherian models for the evolution of sexual ornaments. The same should also be true for traits that evolve via pleiotropy (e.g., due to sensory exploitation or bias) with no subsequent evolution of condition dependent modification. We collected information on the relationship between traits correlated with male mating rate and estimates of adult male survivorship or life span. In total we obtained 122 samples from 69 studies of 40 species of bird, spider, insect, and fish. In a meta-analysis we calculated the average sample size weighted correlation between trait expression and adult survival. Analyses at the level of samples, studies, and species revealed significant positive relationships (r = 0.08, 0.10, and 0.13, respectively; all P < 0.001). The unweighted correlation at the species level was r = 0.24. In general, males with larger ornaments or weapons, greater body size, or higher rates of courtship showed greater survivorship or longevity. This finding is inconsistent with pure Fisherian models or other models that do not incorporate condition or quality dependent trait expression. It suggests that male investment in sexually selected traits is not fixed but varies in relation to the ability to pay the underlying costs of expressing these characters. Hence, many secondary sexual characters are likely to be condition dependent in their expression.

The origin of the attine ant-fungus mutualism.

Abstract: Cultivation of fungus for food originated about 45-65 million years ago in the ancestor of fungus-growing ants (Formicidae, tribe Attini), representing an evolutionary transition from the life of a hunter-gatherer of arthropod prey, nectar, and other plant juices, to the life of a farmer subsisting on cultivated fungi. Seven hypotheses have been suggested for the origin of attine fungiculture, each differing with respect to the substrate used by the ancestral attine ants for fungal cultivation. Phylogenetic information on the cultivated fungi, in conjunction with information on the nesting biology of extant attine ants and their presumed closest relatives, reveal that the attine ancestors probably did not encounter their cultivars-to-be in seed stores (von Ihering 1894), in rotting wood (Forel 1902), as mycorrhizae (Garling 1979), on arthropod corpses (von Ihering 1894) or ant faeces in nest middens (Wheeler 1907). Rather, the attine ant-fungus mutualism probably arose from adventitious interactions with ...

Photoperiodic polyphenisms in rodents: neuroendocrine mechanisms, costs, and functions.

Abstract: Annual changes in daylength figure prominently in the generation of seasonal rhythms in reproduction, and a wide variety of mammals use ambient photoperiod as a proximate cue to time critical reproductive events. Nevertheless, within many reproductively photoperiodic mammalian species, there exist individuals--termed "photoperiod nonresponders"--that fail to adopt a seasonal breeding strategy and instead exhibit reproductive competence at a time of year when their conspecifics are reproductively quiescent. Photoperiod nonresponsiveness has been principally characterized by laboratory observations--over half of the species known to be reproductively photoperiodic contain a proportion of nonresponsive individuals. The study of nonresponders has generated basic insights regarding photic regulation of reproduction in mammals. The neuroendocrine mechanisms by which the short-day photoperiodic signal is degraded or lost in nonresponders varies between species: differences in features of the circadian pacemaker, which provides photoperiodic input to the reproductive neuroendocrine system, have been identified in hamsters; changes in the responsiveness of hypothalamic gonadotrophs to melatonin and as-yet-unspecified inhibitory signals have been implicated in voles and mice. Individuals that continue to breed when their conspecifics refrain might enjoy higher fitness under certain circumstances. Statements regarding the adaptive function of reproductive nonresponsiveness to photoperiod require additional information on the costs (metabolic and fitness) of sustaining reproductive function during the winter months and how these costs vary as a function of environmental conditions. Reproductive nonresponders thus continue to represent a challenge to theories that extol the adaptive function of seasonality. Several nonexclusive hypotheses are proposed to account for the maintenance of nonresponsive individuals in wild rodent populations.

Evolution in health and disease: work in progress.

Abstract: This article surveys progress in Darwinian medicine since 1991. Evolutionary thinking has been providing an increasing flow of fresh ideas into medical science, ideas that would not be suggested by other perspectives. Recent contributions have shed new light on the evolution of virulence, of antibiotic resistance, of oocytic atresia, of menopause, of the timing of the expression of genetic disease, of links between mate choice and disease resistance, and of genomic conflict between mother and fetus over resource provisioning. An important consequence of changes from the environment of evolutionary adaptedness concerns reproductive cancers; the incidence of reproductive cancers may be linked to changes in the frequency of menstruation in postindustrial societies. Other intriguing developments include some unanticipated and undesirable consequences of good hygiene, hope from an unexpected quarter for progress on nerve and muscle regeneration, evolutionary interpretations of mental disease, and insights from functional genomics into the nature of tradeoffs. The application of evolutionary thinking to problems in medical research and practice has thus yielded an abundant and growing harvest of insights. Some are well founded, others remain speculative. The field is moving from an initial phase dominated by speculation and hypothesis formation into a more rigorous phase of experimental testing of explicit alternatives. Currently the most promising areas, those in which experimental rigor can be applied efficiently, include experimental evolution and functional genomics. The pioneers can be proud of what they have set in motion.

Evolution in changing environments: the "synthetic" work of Clausen, Keck, and Hiesey.

Abstract: The studies of Clausen, Keck, and Hiesey (CKH) have been widely cited as exemplars of ecotypic differentiation in textbooks and in the primary literature. However, the scope of their findings and achievements is significantly greater than this. In this paper we analyze the research program of CKH, highlighting their major findings during the years when the modern synthesis of evolution was taking shape. That synthesis, curiously, drew little from their examples, although their studies at the Carnegie Institution represent conceptual and methodological work that is still relevant. The works of CKH not only embodied the principles of the nascent synthesis, but often provided needed supporting data. Their classic work, especially on Achillea and Potentilla, produced abundant evidence on population differentiation of many quantitative traits and plant phenotypes, as well as demonstrating the now commonly reported distinction between environmental and genetic determination of traits. Their ecological genetic investigations of quantitative traits in plants were in sharp contrast to contemporaneous animal studies on adaptation that focused on discrete polymorphisms--with correspondingly little influence of the environment on phenotypic expression. Of utmost importance was the demonstration by CKH of adaptive differentiation by natural selection and their approaches to understanding the genetic structure of populations.

The hormetic zone: an ecological and evolutionary perspective based upon habitat characteristics and fitness selection.

Abstract: Fitness varies nonlinearly with environmental variables such as temperature, water availability, and nutrition, with maximum fitness at intermediate levels between more stressful extremes. For environmental agents that are highly toxic at exposures that substantially exceed background levels, fitness is maximized at concentrations near zero-a phenomenon often referred to as hormesis. Two main components are suggested: (1) background hormesis, which derives from the direct adaptation of organisms to their habitats; and (2) stress-derived hormesis, which derives from metabolic reserves that are maintained as an adaptation to environmental stresses through evolutionary time. These reserves provide protection from lesser correlated stresses. This article discusses illustrative examples, including ethanol and ionizing radiation, aimed at placing hormesis into an ecological and evolutionary context. A unifying approach comes from fitness-stress continua that underlie responses to abiotic variables, whereby sele...

Evolutionary Biology: Struggling to Escape Exclusively Individual Selection

Abstract: LEVELS OF SELECTION IN EVOLUTION. Monographs in Behavior and Ecology. Edited by Laurent Keller. Princeton (New Jersey): P7inceton University Press. $59.50 (hardcover); $16.95 (paper). xii + 318 p; ill.; author and subject indexes. ISBN: 0-691-00703-9 (hc); 0-69100704-7 (pb). 1999. '71 ,/fANY AN ecologist, equipped with no more than a flimsy analogy, marched cheerfully from thefamiliarDarwinian territory of individual organisms into a world of populations and groups. Populations were treated as individuals that just happened to be a notch or two up in the hierarchy of life\" (Cronin 1991, p 278). \"The major transitions in evolutionary units are from individual genes to networks of genes, from gene networks to bacterialike cells, from bacterialike cells to eukaryotic cells with organelles, from cells to multicellular organisms, and from solitary organisms to societies\" (Keller 1999, p 60). The first passage quoted above is a description of the bad old days, before the theory of individual selection (or is it gene selection?) became the reigning paradigm in evolutionary biology. The second passage is from a chapter of a new edited volume, Levels of Selection in Evolution. Far from being a bunch of heretics, the contributors include some of the most distinguished names in current evolutionary biology. This volumejoins a number of other books (Maynard Smith and Szathm'ary 1995; Seeley 1995; Frank 1998; Sober and Wilson 1998; Boehm 1999; Michod 1999) and special issues of journals (American Naturalist 1997; Human Nature 1999) on evolution as a multilevel process. Clearly, something has happened to make the bad old days look like the wave of the future. Unfortunately, like a butterfly struggling to emerge from its pupal skin, Levels of Selection in Evolution presents an awkward picture of multilevel selection. Some chapters are excellent, but others are highly ambivalent and, in some cases, downright confused about what multilevel selection is and how it relates to its own past. It will be helpful to summarize the theory before evaluating the strengths and weaknesses of this particular volume.

The science of Louis Pasteur: a reconsideration.

Abstract: O NJUNE 13, 1895, Louis Pasteur retired to Villeneuve-L'Etang, near Paris, where the stables that were once part of Napoleon III's mounted guard were being used to obtain antidiphtheria serum. The cerebrovascular ischemia which had left him hemiplegic on the left side since he was 46 had worsened. The great biography of Pasteur, published in 1900 by his son-in-law Rene Vallery-Radot, describes the end this way: