Social Information on Fear and Food Drives Animal Grouping and Fitness.

Empirical studies in select systems suggest that social information-the incidental or deliberate information produced by animals and available to other animals-can fundamentally shape animal grouping behavior. However, to understand the role of social information in animal behavior and fitness, we must establish general theory that quantifies effects of social information across ecological contexts and generates expectations that can be applied across systems. Here we used dynamic state variable modeling to isolate effects of social information about food and predators on grouping behavior and fitness. We characterized optimal behavior from a set of strategies that included grouping with different numbers of conspecifics or heterospecifics and the option to forage or be vigilant over the course of a day. We show that the use of social information alone increases grouping behavior but constrains group size to limit competition, ultimately increasing individual fitness substantially across various ecological contexts. We also found that across various contexts, foraging in mixed-species groups is generally better than foraging in conspecific groups, supporting recent theory on competition-information quality trade-offs. Our findings suggest that multiple forms of social information shape animal grouping and fitness, which are sensitive to resource availability and predation pressure that determine information usefulness.

Effects of population density on corticosterone levels of prairie voles in the field.

High population density is often associated with increased levels of stress-related hormones, such as corticosterone (CORT). Prairie voles (Microtus ochrogaster) are a socially monogamous species known for their large population density fluctuations in the wild. Although CORT influences the social behavior of prairie voles in the lab, the effect of population density on CORT has not previously been quantified in this species in the field. We validated a non-invasive hormone assay for measuring CORT metabolites in prairie vole feces. We then used semi-natural enclosures to experimentally manipulate population density, and measured density effects on male space use and fecal CORT levels. Our enclosures generated patterns of space use and social interaction that were consistent with previous prairie vole field studies. Contrary to the positive relationship between CORT and density typical of other taxa, we found that lower population densities (80 animals/ha) produced higher fecal CORT than higher densities (240/ha). Combined with prior work in the lab and field, the data suggest that high prairie vole population densities indicate favorable environments, perhaps through reduced predation risk. Lastly, we found that field animals had lower fecal CORT levels than laboratory-living animals. The data emphasize the usefulness of prairie voles as models for integrating ecological, evolutionary, and mechanistic questions in social behavior.

Extreme gender flexibility: using a phylogenetic framework to infer the evolution of variation in sex allocation, phylogeography, and speciation in a genus of bidirectional sex changing fishes(Lythrypnus, Gobiidae).

The genus Lythrypnus is a group of marine gobies that exhibit extreme gender flexibility as bidirectional sex changers. The genus consists of 20 described species and several undescribed species that are distributed in the Americas. Five species have been characterized with respect to sex allocation and gonad morphology. The hormonal, morphological, and behavioral aspects of sex change have been studied extensively for one species, L. dalli. These data, however, have not been interpreted in an evolutionary context because a phylogenetic hypothesis has not previously been proposed for the genus Lythrypnus. We propose the first phylogenetic hypothesis for the genus based on molecular data from three mitochondrial genes (12s, ND2, and Cytb), one nuclear gene (Rag1) and one nuclear intron (S7). We also include three previously undescribed Lythrypnus species. Our results support the monophyly of the genus with L. heterochroma, an Atlantic species, as the basal taxon. After the divergence of L. heterochroma, there are two main clades, one comprised of species distributed in the Atlantic, the other comprised of species distributed in the Pacific. These data indicate an Atlantic origin for the genus, followed by divergence after the closure of the Isthmus of Panama. Our data also support the monophyly of three previously described species complexes, the L. rhizophora complex and L. dalli complex in the Pacific, and the L. mowbrayi complex in the Atlantic. We mapped patterns of sex allocation within this genus onto the fully resolved and supported topology, and found that sexual plasticity and gender flexibility is likely a synapomorphy for the genus. Overall our results create a well-supported framework to understand the phylogeography of the genus, and to interpret the evolution of sex allocation in Lythrypnus gobies.

Leaf-footed bugs possess multiple hidden contrasting color signals, but only one is associated with increased body size.

Antipredatory displays that incorporate hidden contrasting coloration are found in a variety of different animals. These displays are seen in organisms that have drab coloration at rest, but when disturbed reveal conspicuous coloration. Examples include the bright abdomens of mountain katydids and the colorful underwings of hawk moths. Such hidden displays can function as secondary defenses, enabling evasion of a pursuant predator. To begin to understand why some species have these displays while others do not, we conducted phylogenetic comparative analyses to investigate factors associated with the evolution of hidden contrasting coloration in leaf-footed bugs. First, we investigated whether hidden contrasting coloration was associated with body size because these displays are considered to be more effective in larger organisms. We then investigated whether hidden contrasting coloration was associated with an alternative antipredatory defense, in this case rapid autotomy. We found that leaf-footed bugs with hidden contrasting coloration tended to autotomize more slowly, but this result was not statistically significant. We also found that the presence of a body size association was dependent upon the form of the hidden color display. Leaf-footed bugs that reveal red/orange coloration were the same size, on average, as species without a hidden color display. However, species that reveal white patches on a black background were significantly larger than species without a hidden color display. These results highlight the diversity of forms that hidden contrasting color signal can take, upon which selection may act differently.

The evolution of autotomy in leaf-footed bugs.

Sacrificing body parts is one of many behaviors that animals use to escape predation. This trait, termed autotomy, is classically associated with lizards. However, several other taxa also autotomize, and this trait has independently evolved multiple times throughout Animalia. Despite having multiple origins and being an iconic antipredatory trait, much remains unknown about the evolution of autotomy. Here, we combine morphological, behavioral, and genomic data to investigate the evolution of autotomy within leaf-footed bugs and allies (Insecta: Hemiptera: Coreidae + Alydidae). We found that the ancestor of leaf-footed bugs autotomized and did so slowly; rapid autotomy (<2 min) then arose multiple times. The ancestor likely used slow autotomy to reduce the cost of injury or to escape nonpredatory entrapment but could not use autotomy to escape predation. This result suggests that autotomy to escape predation is a co-opted benefit (i.e., exaptation), revealing one way that sacrificing a limb to escape predation may arise. In addition to identifying the origins of rapid autotomy, we also show that across species variation in the rates of autotomy can be explained by body size, distance from the equator, and enlargement of the autotomizable appendage.

Agriculture alters gonadal form and function in the toad Bufo marinus.

BACKGROUND: Many agricultural contaminants disrupt endocrine systems of wildlife. However, evidence of endocrine disruption in wild amphibians living in agricultural areas has been controversial. Typically, studies on the effects of pollutants on wildlife attempt to compare polluted with unpolluted sites. OBJECTIVES: We took a novel approach to address this question by explicitly quantifying the relationship between gonadal abnormalities and habitats characterized by differing degrees of agricultural activity. METHODS: We quantified the occurrence of gonadal abnormalities and measures of gonadal function in at least 20 giant toads (Bufo marinus) from each of five sites that occur along a gradient of increasing agricultural land use from 0 to 97%. RESULTS: The number of abnormalities and frequency of intersex gonads increased with agriculture in a dose-dependent fashion. These gonadal abnormalities were associated with altered gonadal function. Testosterone, but not 17beta-estradiol, concentrations were altered and secondary sexual traits were either feminized (increased skin mottling) or demasculinized (reduced forearm width and nuptial pad number) in intersex toads. Based on the end points we examined, female morphology and physiology did not differ across sites. However, males from agricultural areas had hormone concentrations and secondary sexual traits that were intermediate between intersex toads and non-agricultural male toads. Skin coloration at the most agricultural site was not sexually dimorphic; males had female coloration. CONCLUSIONS: Steroid hormone concentrations and secondary sexual traits correlate with reproductive activity and success, so affected toads likely have reduced reproductive success. These reproductive abnormalities could certainly contribute to amphibian population declines occurring in areas exposed to agricultural contaminants.

Quantifying site quality in a heterogeneous landscape: recruitment of a reef fish.

Heterogeneity in site quality can play an important role in patterns of abundance and population dynamics. Yet, estimating site quality in natural systems can be problematic because site quality can (1) vary through ontogeny for a focal organism, leading to shifts in site quality with age, (2) be confounded with (or masked by) variation in traits of individuals populating the sites, and (3) be correlated with local density. For example, if high-quality sites attract more individuals but vital rates are density dependent, then observed vital rates will be relatively homogeneous in space despite strong heterogeneity in site quality. Here, we operationally define site quality for a reef fish as the mean survival time of juveniles transplanted to sites at a common density and size structure, with random assignment of individuals to sites to remove potential confounding effects of local variation in individual quality and density. Our assays using juvenile age classes of the six-bar wrasse (Thalassoma hardwicke) showed that site quality varied in space (i.e., among patch reefs) but was constant through time. Site quality increased with availability of the branching coral Pocillopora (which is used as a refuge), but decreased with density of a predator, the arc-eye hawkfish, Paracirrhites arcatus (which also uses Pocillopora). We experimentally added colonies of Pocillopora to reefs and (1) increased site quality, (2) enhanced natural settlement rates of six-bar wrasse, but (3) attracted more hawkfish predators, and (4) did not increase survival of juvenile fish under ambient densities. Our results suggest that Pocillopora increases site quality, but attracts greater densities of settlers and predators, resulting in increased density dependence and predation, which mask the underlying effects of Pocillopora on site quality (supporting the hypothesis of "cryptic density dependence"). Variation in site quality and the possible confounding effects of density and individual traits warrant more experimental study.

Renal pathologies in giant toads (Bufo marinus) vary with land use.

A variety of human land uses involve the release of toxins into the environment. Wildlife live alongside humans across this array of land uses and thus, are exposed to varying chemical milieus. Kidneys are the principle excretory organs for vertebrates and excessive or chronic exposure to exogenous toxins can lead to renal pathology and renal failure. Although studies have linked chemical exposure to specific renal diseases across diverse taxa, none compare renal lesions occurring in wildlife living in different types of human-modified landscapes. We identify lesions characteristic of renal stress, including toxin exposure, in 82 giant toad (Bufo marinus) males living in habitats ranging from suburban to agricultural. In a previous study [McCoy K.A., Bortnick L.J., Campbell C.M., Hamlin H.J., Guillette L.J., Jr., St. Mary C.M. Agriculture Alters Gonadal Form and Function in Bufo marinus. Environ Health Persp; in press.], these individuals were examined for gonadal abnormalities, which were significantly and positively associated with percentage of agriculture at the collection site. Thus, we hypothesized the same association for renal abnormalities. We scored gross anatomical abnormalities and used light microscopy to identify tubular and interstitial lesions that have been associated with toxicant exposure in other organisms, including humans. Renal lesions indicative of tubular disease were observed at one suburban and two agricultural sites, whereas interstitial lesions were most severe at one agricultural site. Although there was no relationship between frequency of renal disease and proportion of agriculture in the collection vicinity, the renal lesions we identify are consistent with toxin exposure and are similar to those found in human drug abusers and patients suffering medication-induced nephropathy. This is the first study to describe renal lesions in a wild amphibian species and investigate the distribution of renal lesions across human altered landscapes. Indentifying the chemicals inducing renal lesions across these landscapes, their toxicological mechanisms, and their implications on wildlife health will help us devise strategies to mitigate the impacts of toxins on humans and animals living in human-modified environments.

Cut your losses: self-amputation of injured limbs increases survival.

Autotomy, self-induced limb loss, is an extreme trait observed throughout the animal kingdom; lizards drop their tails, crickets release their legs, and crabs drop their claws. These repeated evolutionary origins suggest that autotomy is adaptive. Yet, we do not have a firm understanding of the selective pressures that promote and maintain this extreme trait. Although multiple adaptive hypotheses exist, research has generally focused on autotomy's adaptive value as a form of predator escape. However, autotomy could also be selected to reduce the cost of an injured limb, which we investigate here. Previously, this alternative hypothesis has been challenging to directly test because when an injury occurs on an autotomizable limb, that limb is almost always dropped (i.e., autotomy is behaviorally fixed within populations). Recently, however, we have identified a species, Narnia femorata (Insecta: Hemiptera: Coreidae), where some individuals autotomize limbs in response to injury, but some do not. This natural variation allowed us to investigate both the survival costs of retaining an injured limb and the benefits of autotomizing it. In this study, we find a positive association between autotomizing injured limbs and survival, thereby quantifying a new and likely widespread benefit of autotomy-reducing the cost of injury.

The evolutionary trade-off between stem cell niche size, aging, and tumorigenesis.

Many epithelial tissues within multicellular organisms are continually replenished by small independent populations of stem cells largely responsible for maintaining tissue homeostasis. These continually dividing populations are subject to mutations that can lead to tumorigenesis but also contribute to aging. Mutations accumulate in stem cell niches and change the rate of cell division and differentiation; the pace of this process and the fate of specific mutations depend strongly on niche population size. Here, we create a mathematical model of the intestinal stem cell niche, crypt system, and epithelium. We calculate the expected effect of fixed mutations in stem cell niches and their effect on tissue homeostasis throughout the intestinal epithelium over organismal lifetime. We find that, due to the small population size of stem cell niches, mutations predominantly fix via genetic drift and decrease stem cell fitness, leading to niche and tissue attrition, and contributing to organismal aging. We also explore mutation accumulation at various stem cell niche sizes and demonstrate that an evolutionary trade-off exists between niche size, tissue aging, and the risk of tumorigenesis. Further, mouse and human niches exist at a size that minimizes the probability of tumorigenesis, at the expense of accumulating deleterious mutations due to genetic drift. Finally, we show that the trade-off between the probability of tumorigenesis and the extent of aging depends on whether or not mutational effects confer a selective advantage in the stem cell niche.

Giant toads (Rhinella marina) living in agricultural areas have altered spermatogenesis.

Across diverse taxa, germ cell development is controlled by an intricate cascade of processes that are tightly controlled by the hypothalamic-pituitary-gonadal axis. Endocrine disturbances, such as those induced by endocrine disrupting chemicals (EDCs) can negatively affect spermatogenesis. Here, we investigate whether spermatogenesis is altered in the giant toad, Rhinella marina, living in agricultural areas where EDCs are used relative to suburban areas. We also ask if reductions in spermatogenesis were associated with developmental gonadal abnormalities (intersex) found in the same frogs. We found that toads in agricultural areas exhibited reduced spermatogenesis relative to non-agricultural animals, and that those reductions were not associated with gross gonadal abnormalities. All toads living in agricultural areas had reduced spermatogenesis relative to those living in non-agricultural areas regardless of whether they had gonadal abnormalities originating during development. Similarities in reproductive dysfunction among diverse taxa living in agricultural areas, including humans, suggest that many vertebrate taxa living in agricultural areas around the globe are likely experiencing some level of reproductive dysfunction.

Parents benefit from eating offspring: density-dependent egg survivorship compensates for filial cannibalism.

Why should animals knowingly consume their own young? It is difficult to imagine many circumstances in which eating one's own young (i.e., filial cannibalism) actually increases an individual's fitness; however, filial cannibalism commonly co-occurs with parental care in fishes. The evolutionary significance of filial cannibalism remains unclear. The most commonly accepted explanation is that filial cannibalism is a mechanism by which caring males gain energy or nutrients that they reinvest into future reproduction, thereby increasing net reproductive success. There is mixed support for this hypothesis and, at best, it can only explain filial cannibalism in some species. A recent alternative hypothesis suggests that filial cannibalism improves the survivorship of remaining eggs by increasing oxygen availability, and thus increases current reproductive success. This theory has received little attention as of yet. We evaluated the hypothesis of oxygen-mediated filial cannibalism in the sand goby by examining the effect of oxygen and egg density on the occurrence of filial cannibalism, evaluating the effects of partial clutch cannibalism on the survivorship of remaining eggs, and comparing potential costs and benefits of filial cannibalism related to the net number of eggs surviving. Indeed, we found that oxygen level and egg density affected the occurrence of cannibalism and that simulated partial clutch cannibalism improved survivorship of the remaining eggs. Additionally, because increased egg survivorship, stemming from partial egg removal, compensated for the cost of cannibalism (i.e., number of eggs removed) at a range of cannibalism levels, filial cannibalism potentially results in no net losses in reproductive success. However, oxygen did not affect egg survivorship. Thus, we suggest a more general hypothesis of filial cannibalism mediated by density-dependent egg survivorship.

The implications of small stem cell niche sizes and the distribution of fitness effects of new mutations in aging and tumorigenesis.

Somatic tissue evolves over a vertebrate's lifetime due to the accumulation of mutations in stem cell populations. Mutations may alter cellular fitness and contribute to tumorigenesis or aging. The distribution of mutational effects within somatic cells is not known. Given the unique regulatory regime of somatic cell division, we hypothesize that mutational effects in somatic tissue fall into a different framework than whole organisms; one in which there are more mutations of large effect. Through simulation analysis, we investigate the fit of tumor incidence curves generated using exponential and power-law distributions of fitness effects (DFE) to known tumorigenesis incidence. Modeling considerations include the architecture of stem cell populations, that is, a large number of very small populations, and mutations that do and do not fix neutrally in the stem cell niche. We find that the typically quantified DFE in whole organisms is sufficient to explain tumorigenesis incidence. Further, deleterious mutations are predicted to accumulate via genetic drift, resulting in reduced tissue maintenance. Thus, despite there being a large number of stem cells throughout the intestine, its compartmental architecture leads to the accumulation of deleterious mutations and significant aging, making the intestinal stem cell niche a prime example of Muller's Ratchet.

Tradeoffs between somatic and gonadal investments during development in the African clawed frog (Xenopus laevis).

Tradeoffs between time to and size at metamorphosis occur in many organisms with complex life histories. The ability to accelerate metamorphosis can increase survival to the next life stage, but the resulting smaller size at metamorphosis is often associated with lower post-metamorphic survival or reduced fecundity of adults. Reduced fecundity is thought to be because of reduced energy reserves, longer time to maturity, or reduced capacity to carry eggs or compete for mates. This pattern could also be explained by a shift in allocation to somatic growth that further retards the growth or development of reproductive tissues. The main goal of this study was to determine if the relationship between growth and development of somatic and gonadal tissues depends on environmental conditions. We address this question through two experiments in which we quantify the development and growth of the body and gonads of Xenopus laevis reared in different resource environments. First, tadpoles were reared communally and development and growth were evaluated over time. Restricted food reduced somatic and gonadal growth rate, but did not affect the developmental rate of either tissue type. Second, tadpoles were reared individually and evaluated at metamorphosis. Restricted food reduced somatic development and growth, but only influenced size, and not developmental stage of testes at metamorphosis. This work demonstrates that environmental conditions influence tradeoffs between growth and development of somatic and gonadal tissues, apparently in a sex-specific manner. These tradeoffs may contribute to phenotypic correlations between small size and reduced fitness.