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Lay Summaries Archive

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Fluctuating asymmetry indicates the optimization of growth rate over developmental stability

Molly R. Morris, Oscar Rios-Cardenas, Susan M Lyons, M. Scarlett Tudor and Lisa M. Bono

Females of many different species prefer to mate with symmetrical males. It has been hypothesized that the degree of asymmetry (how different one side of the body is from the other) is a cue that reliably indicates the genetic ability of an organism to develop correctly even in a poor environment. However, evidence that symmetry provides information about a potential mate's genetic propensity to develop well has been inconsistent, suggesting that we still do not understand why some individuals are more asymmetrical than others.

We examined the hypothesis that asymmetry is an indicator of a male's growth strategy in a swordtail fish. Most males in this species are genetically programmed to stop growing when they reach a certain size, with the time it takes males to reach that size depending on the environment. Some males grow as fast as possible regardless of the environment, and we show in the current study that these males are more often asymmetrical for a pigment pattern of vertical bars (the number of bars on the left side was not equal to the number of bars on their right side). When we raised siblings on high and low quality diets, we documented that these males grew faster than the other males, and there was a relationship between how fast they grew and how asymmetrical they were.

Our results suggest a hypothesis to explain the inconsistent relationship between asymmetry and environmental stress. Not all individuals will have the same growth strategy, such that some will grow slower when the environment is stressful so that they can still grow well (develop symmetrically), while others will continue to grow fast in the stressful environment, but grow poorly (develop asymmetrically). Once differences in how individual growth rate responds to stress is accounted for, we predict that the relationship between asymmetry and growth rates will be detected in other species as well. Finally, we found that the females of the swordtail fish we studied have a strong mating preference for males with the same number of bars on both sides. And yet, our results can explain why the larger females of some species of swordtail fishes have been shown to prefer asymmetrical males. In some conditions, choosing a mate that grows fast even if it means they have grown poorly (are asymmetrical) may be adaptive.

Image caption: Male swordtail fish with an asymmetrical vertical bar pigment pattern; (TOP) 5 bars on left and (BOTTOM) 6 bars on right. Courtesy of Molly R Morris.

 

Variation in monsoon precipitation drives spatial and temporal patterns of Larrea tridentata growth in the Sonoran Desert

Ryan A. Sponseller, Sharon J. Hall, David Huber, Nancy B. Grimm, Jason P. Kaye, Christopher M. Clark and Scott L. Collins

Variation in plant growth across multiple biomes is influenced by the distribution and characteristics of rainfall. The ecological relevance of precipitation patterns is particularly clear for arid and semi-arid regions where growth is limited by water availability. Despite this recognition and a long history of research, our ability to predict patterns of desert plant growth, and understand how these ecosystems may be influenced by a changing climate, remains incomplete. One important challenge is to better understand how desert plants respond to different aspects of the annual precipitation regime, including variation in the amount and characteristics of rainfall in different seasons.

We evaluated patterns of stem growth by the shrub, creosotebush (Larrea tridentate), over a 5-year period in the northern Sonoran Desert of central Arizona (2006-2010). Creosotebush is a dominant perennial shrub in the warm deserts of the southwestern US and Mexico. Across much of this range, creosotebush receives rainfall during both winter/spring and summer monsoons seasons, yet which of these seasons is most important for growth is unclear. We took advantage of a large dataset on stem growth associated with these two major rainfall seasons from 60 plots located in and around the Phoenix metropolitan area. We observed both the highest and lowest rates of growth during the summer, with large increases in growth when seasonal monsoon rainfall exceeded 100 mm. We found that growth during the winter/spring rainy season was intermediate in magnitude, and did not differ much among years even though winter/spring rainfall did vary. Growth of creosotebush also varied from place to place, both among sites having different amounts of rainfall and among plants at each site that experienced the same climatic conditions. This spatial variation was much greater during summer than in the winter/spring period. Overall, results highlight the sensitivity of both the magnitude and spatial heterogeneity of creosotebush growth to variation in seasonal precipitation. Specifically, our work suggests that small changes in the character of the summer monsoon could have important consequences for the growth of this long-lived perennial shrub.

Image caption: Sonoroan Desert National Monument (Arizona, USA. Coutresy of David P. Huber.

 

Fine-scale local adaptation in life histories along a continuous environmental gradient in Trinidadian guppies

Julián Torres-Dowdall, Corey Handelsman, Emily Ruell, Sonya Auer, David Reznick and Cameron Ghalambor

Mortality caused by predators is thought to be an important driver of the evolution of life histories. Populations of prey that co-occur with predators are predicted to mature younger and smaller, reproduce more frequently, and invest proportionally more energy in each reproductive event than those that live in predator-free environments. Testing these predictions requires the comparison of multiple populations of one species experiencing different levels of predation risk. Several studies in plants and animals have provided support for these predictions. However, most of these studies have contrasted only populations that experience high versus low levels of predation. By comparing multiple populations along gradients of predation risk, we can gain understanding of the scale at which adaptation to the predator environment occurs.

Here, we examined life-history traits along a gradient of predation pressure in the Trinidadian guppy (Poecilia reticulate). In streams on the island of Trinidad, downstream communities are complex and include several species of predatory fishes. However, waterfalls function as barriers to the upstream dispersal of predators, resulting in a stepwise deletion of predatory species as we move upstream. Headwater tributaries are relatively simple communities with lower predation risk for guppies.

We sampled guppies from six populations along this gradient of predation pressure and compared their life-history traits. As we expected, there was a gradual change in life-history characteristics that paralleled the gradual change in predator diversity. Females collected from downstream populations that coexist with more predators allocated proportionally greater energy to reproduction by producing more, smaller offspring than we found in upstream populations. Also, by rearing all six populations for two generations under common conditions in the laboratory, we demonstrated that the observed variation in life-history traits had a genetic basis.

Our results imply that local adaptation in guppies occurs at a finer scale than has previously been shown. Furthermore, while our results are consistent with predator-driven life-history variation, we also find patterns of plasticity that would not be apparent in the traditional dichotomous comparison of populations at the extremes of this continuum (high versus low) of predation risk.

Image caption: Wild male and female guppies. Coutresy of Paul Bentzen.

 

Testing metabolic theory with models of tree growth that include light competition

Nadja Rüger and Richard Condit

A well-established theory of physiology explains how the rate of metabolism increases as individuals grow, and it even applies to humans: heavier people use more energy than small people, but less when measured per body weight. Mathematically speaking, we find that, on average, a 100% increase in body weight leads to a 59% increase in energy use in many organisms.

The focus of our current study was a test of how this rule applies to different tree species in a diverse forest in Panama, where 300 tree species grow together. Our research is about the metabolism of tree species in this rainforest. Plants use sunlight to build sugars, then consume sugars to generate energy needed for growth and reproduction. We measure the growth of forests and partition it among individuals and species. The largest trees, of course, produce the most biomass, whereas seedlings and saplings contribute little. Studying how biomass production increases as trees grow helps us understand why some forests are more productive than others, and can be used to manage productivity in plantations.

The basics of the metabolic theory apply to all species equally, however species sharing a forest may adopt different strategies for absorbing sunlight and growing roots and leaves. We use modern, advanced statistical methods that permit every species to be studied in detail while also examining the overall average behavior of the forest. We found that the fundamental metabolic rule (59% increase per doubling of weight) does indeed apply at the average level, but only for trees growing in sufficient light, and that individual species vary widely around this average, some well below and some above. This result leads us to ask why they vary, and also suggests how to increase productivity by selecting species exceeding the theoretical prediction.

Image caption: Cedrela odoratasapling growing towards the light. Coutresy of Nadja Rüger.

 

Growth hormone reduces growth in free-living Atlantic salmon fry

Line Sundt-Hansen, Sigurd Einum, Lena Neregård, Björn Björnsson, Jörgen Johnsson, Ian Fleming, Robert Devlin and Kjetil Hindar

Published on: 10th May 2012

Juvenile Atlantic salmon face highmortality due to predation, starvation and fierce competition. Fast growth has been assumed to be beneficial as reaching a larger size earlier would reduce risk of predation and provide a size benefit in competition with other juveniles. Such rapid growth is strongly associated with increased levels of growth hormone (GH) in fish, as well as in most other vertebrates. On the other hand, increased GH levels may have costs such as reduced anti-predator behaviour, reduced starvation tolerance and decreased longevity.

We investigated trade-offs related to an increased GH level in very young juvenile Atlantic salmon. Atlantic salmon fry were given GH implants or a placebo treatment, then. released into a natural river.Fish with the same type of treatment were also kept in indoor hatchery tanks to observe their growth. After two months the fish in the indoor tanks that had received GH implants showed a far better growth than those with a placebo treatment. However, surprisingly, the fish that had been in the river showed exactly the opposite pattern. In contrast, previous studies conducted at later developmental stages had showed a positive growth effect or no effect of GH implants.

The unexpected result shows that the same GH treatment may cause completely different results given different conditions. Thus, the optimal growth rate in a certain environment may not necessarily be the maximum growth rate possible, indicating trade-offs and costs related to an increased GH level.

This study provides important knowledge for the ecological risk assessment of genetically modified salmon. Increasing the GH level in salmon simulates genetically modified salmon, which have a higher GH level than wild salmon. Realistic experiments of transgenic fish are difficult due to the need for strict containment. This study showed that transgenic salmon at a very early life stage may actually be less competitive than their wild conspecifics, given the same environmental conditions. However, GH cannot fully imitate transgenic fish, as transgenic fish would experience a lifetime of exposure to elevated GH levels, compared to GH implanted fish experiencing elevated levels for a limited time.

Image caption: Juvenile Atlantic salmon resting on the river bed. Courtesy of Sundt-Hansen.

 

No evidence that temperature related fertility differences influence the distribution of a selfish genetic element

Tom Price, Robin Hoskyn, Hannah Rapley, Julian Evans and Nina Wedell

Published on: 15th March 2012

During sperm production, every chromosome normally has a 50% chance of making it into each sperm cell. However, some chromosomes selfishly cheat to ensure that they get into all sperm, eliminating those carrying the alternative chromosome. This increases the success of the cheating chromosome (called a 'meiotic driver'), allowing it to spread through populations. If the cheating chromosome also determines the sex of the individual that carries it (like an X or Y in humans), this can lead to populations of predominantly one sex. In extreme cases this could wipe out the population, due to the lack of one sex.

However, in natural populations such 'sex ratio distorting meiotic drivers' are typically found at stable frequencies. Moreover, the examples where we have the best distribution data (from North America and Europe) show that they are commonest in southern populations, and are rare or absent in the north. No one knows why.

One possibility is temperature. Low temperature is well known to damage sperm production. Meiotic drivers also frequently damage sperm, because they kill the sperm that carry the alternative chromosomes. If the damage from extreme temperature and meiotic drive combine, meiotic drive males may be unable to mate successfully in the north, explaining the distribution.

We tested this in the fruit fly Drosophila pseudoobscura that carries the meiotic driver 'SR' (sex ratio). The frequency of SR increases from Canada(0.1%) south to Mexico (30%), a distribution that has been stable for at least 50 years. We kept flies at three temperatures, from hot to cold. We examined sperm production by mating each male to as many females as possible over two days, and examined the number of offspring produced. We also examined the rates of male infertility at each temperature for males carrying SR and normal males. Contrary to our predictions, we found that low temperatures had little impact. Instead, meiotic drive males had low sperm production and high rates of infertility at high temperatures. Hence this interaction cannot explain the distribution of SR in nature, which remains a mystery.

Image caption: Drosophila pseudoobscura copulating. Coutresy of Thomas Price.

 

Nesting Tree Swallows "decide" how much weight to lose before they even gain it

Alice Boyle, David Winkler and Christopher Guglielmo

Published on: 10th May 2012

Tree Swallows return every spring to nest across North America, and their aerobatic flights over meadows and lakes embody the freedom of flight. While the flights of swallows may look effortlessly graceful to us, they actually require a tremendous amount of energy. When females must feed half a dozen hungry nestlings, those energetic costs are multiplied. The heavier the mother, the more sluggish she is and the more energy she spends feeding herself and her young. Previous researchers noticed that many female birds lose weight during nesting, but it wasn't known if they lose weight because they're spending more energy to feed their young, or whether they are able to reduce their weight in anticipation of the nestling period, enabling them to be more agile and energy-efficient when foraging demands are high.

To test these alternatives we used new quantitative magnetic resonance technology to precisely measure the fat and lean mass of individual birds through time. We followed twenty females breeding near Ithaca NY from early in incubation to late in nesting when chicks are close to fledging. Because these swallows nest in artificial nest boxes, we could control the timing of measurements, weighing and scanning birds at five times during nesting. The swallows lost weight mostly by losing fat, and they did so quite rapidly around the time their eggs hatched. By the time females were feeding hungry nestlings, they were carrying a minimum of fat, and weighed about the same as females do a month before nesting. The amount of weight each female lost also depended upon how heavy she was to start off with and how many nestlings she had to feed. This means that when females "decide" how many eggs to lay in the spring, they also "decide" how much weight to gain. They appear to anticipate the benefits of storing enough extra fat to carry them through bad weather when they can't feed, but can minimize the costs by losing most of that extra weight when their eggs hatch, being light on the wing when efficiency becomes more important.

Image caption: Alice Boyle opens a nest box to count the number of chicks being fed by a nesting Tree Swallow near Ithaca, New York. Courtesy of Hope Grietzer.

 

What makes a guppy a guppy?

Rana El-Sabaawi, Eugenia Zandona, Tyler Kohler, Michael Marshall, Jennifer Moslemi, Joseph Travis, Andres Lopez-Sepulcre, Regis Ferriére, Catherine Pringle and Steven Thomas

Published on: 12th March 2012

All animals are composed of similar building blocks including proteins, fats or nucleic acids. These building blocks are made up of elements. Fats, for example, are rich in carbon, and bone is rich in phosphorus. Animals differ in the proportions of these building blocks, and correspondingly in their elemental composition. Animals that have large skeletons have proportionately more phosphorus in their bodies than animals with smaller skeletons. Animals acquire these elements from their diets. If animals do not meet their elemental demands, their growth rates and reproduction may suffer. These physiological consequences can also influence how animals compete with other animals, or how animals interact with their environments. Understanding factors that influence elemental composition of animals is important because it provides insight into a wide range of ecological and environmental processes.

In this study we ask what are the most important predictors of elemental composition (also known as organismal stoichiometry) using the Trinidadian guppy as a model. In Trinidad there are two types (phenotypes) of guppies: those from sites with predators, and those from sites without predators. These phenotypes differ in their growth rate and reproduction. Because these traits may require different proportions of molecules, they may influence the guppy's elemental composition. However, guppies are also widely distributed in different rivers, and environmental differences between rivers may influence the elemental content of guppies because environmental variability ultimately controls the availability of elements.

We find that guppies from different rivers have significantly different elemental composition, and those differences outweigh phenotypic differences in elemental composition. However, the two guppy phenotypes appear to lack different elements from their diets. Guppies from sites with predators lack carbon, while guppies from sites without predators lack phosphorus. Ultimately the elemental composition of guppies appears to be a product of environmental variability in their habitat. Understanding how phenotypic effects on dietary mismatch and spatial effects on elemental composition interact is a new and important challenge.

Image caption: A male and female guppy in a Trinidadian pool. Courtesy of Paul Bentzen.

 

Proximate mechanisms of behavioral inflexibility: implications for the evolution of personality traits

Renee Duckworth and Keith Sockman

Published on: 12th March 2012

It's easy to assume that animals must benefit from flexible behaviour, yet recent studies show that individual animals have definite personalities and show highly repeatable behaviour even under different circumstances. Why is behaviour not more flexible? One possibility is that behaviour cannot be more flexible because it is integrated into other parts of an animal's overall life history which are themselves relatively inflexible. Another possibility is the genes responsible for the behaviour may also have other effects (so-called pleiotropic effects), thus limiting the ability of the behaviour to vary independently.

We investigated these ideas by looking at the mechanisms behind aggressive and non-aggressive personality types in male western bluebirds, Sialia Mexicana. Aggressive individuals have the highest fitness when dispersing and colonizing new habitats where competition is high, but aggressive males that remain in territories adjacent to their relatives have lower fitness than nonaggressive males because they invest less in parental care. Given the cost of aggression, individuals that disperse should remain aggressive while competing for a new territory, but decrease their aggression and focus on parental investment once they have acquired a territory. Because aggression is favourable only some of the time, it is unclear whether consistency in the expression of aggression across all contexts throughout an individual's life is adaptive. On the one hand, it may be adaptive if it is necessary to enable integration of aggression and dispersal. On the other hand, an individual may be consistently aggressive because high levels of male hormones (testosterone) favour extra-pair copulations, even though they also suppress parental behaviour, i.e. aggression is a nonadaptive side-effect of (adaptive) male mating behaviour.

We measured naturally occurring testosterone levels and found that, although testosterone fluctuations determined mating behaviour, e.g., propensity of males to seek mating opportunities, testosterone did not correlate with aggression. In other words, it seems unlikely that an inflexibly aggressive personality is the result of an inevitable hormonal link between aggression and mating behaviour. These results add to a growing body of evidence that the relationship between testosterone and aggression is evolutionarily flexible and, in fact, suggest that decoupling hormones from behaviours is an important prerequisite in the evolution of adaptive personalities.

Image caption: Western bluebirds, Sialia mexicana. Courtesy of Alex Badyaev.

 

The effects of egg yolk and crop milk on the immunity of young pigeons

Lisa Jacquin, Lydie Blottière, Claudy Haussy, Samuel Perret and Julien Gasparini

Published on: 9th May 2012

Vertebrates are able to affect offspring development by transmitting hormones and immune active substances such as antibodies to their young. This is believed to be one way for parents to prepare their offspring for the environmental conditions in which they will grow and has been called 'parental effects'. For instance, the transmission of maternal antibodies through the placenta and milk in mammals, or through the egg yolk in birds, has been shown to increase offspring ability to resist parasites later in life. Indeed, such maternal antibodies are believed to play a pivotal role in offspring development through positive effects on offspring immune system and growth. Some birds such as pigeons, flamingos and penguins are also able to produce a substance in their crop to feed their chicks. This substance has been called 'crop milk' by analogy with mammal milk, but its role in offspring development has remained elusive. In this study, we investigated the respective role of antibodies transmitted through pigeon crop milk or egg yolk on the development of the immune system and growth of young pigeons. By injecting parents either with antigens or with a sham injection (physiological serum), we experimentally created four groups of chicks: 1) chicks receiving antibodies through egg yolk and crop milk; 2) chicks receiving antibodies only through the egg yolk; 3) chicks receiving antibodies only though the crop milk and 4) chicks receiving no antibodies at all. This experimental design enables us to distinguish the effect of maternal antibodies transmitted before birth via the egg yolk or after birth via the crop milk on immunity and growth of the young. First, we found that maternal antibodies transmitted via the egg yolk protected the chicks against an antigen met at early stages. Second, we found that antibodies in crop milk stimulated the immune response of their young after one year of development. This effect depended on the time of early exposure to parasites in young chicks. Pigeon milk could thus have similar immune function as mammalian milk, and is thus an interesting example of the evolution of a system with analogies to mammalian lactation.

Image caption: Feral pigeon Columba livia incubating its eggs. Courtesy of Lisa Jacquin.

 

Geographic variation in vulnerability to climate warming in a tropical Caribbean lizard

Alexander Gunderson and Manuel Leal

Global climate warming is unevenly heating the earth, with temperatures increasing fastest in polar and temperate regions. As a result, studies of the biological impact of warming have focused on polar and temperate animals. However, recent studies have suggested that tropical species may be just as vulnerable to climate warming as their colder-climate counterparts. Surprisingly, few studies have tested this idea rigorously in a tropical species.

We tested vulnerability to climate warming in a tropical lizard, the Puerto Rican crested anole (Anolis cristatellus). The crested anole is a small arboreal species that lives in two distinct habitat types: wet forest and dry forest. We first measured the current thermal environment of this species in each habitat and how thermal environment affects the lizard's body temperature. Then, in the laboratory we measured how body temperature affects the lizard's physiological performance. Next, we calculated how the thermal environment of this species will change after a 3°C increase in air temperature, which is expected in Puerto Rico over the next century. Finally, we tested how the predicted change in thermal environment will affect the lizard's physiological performance.

We found that the crested anole's vulnerability to climate warming is different in each habitat type. After warming, the wet-forest habitat is likely to remain thermally suitable for crested anoles. In contrast, the dry forest habitat is predicted to become too warm, with lizards likely to experience low physiological performance for several hours a day. Thus, dry-habitat lizards will probably have to remain in cool retreats for long periods of the day and greatly reduce activity levels due to warming. Reduced activity (i.e., feeding and mating) can greatly impact reproduction rates, decreasing population sizes and increasing the risk of local extinctions.

Our results provide insights into the vulnerability of cold-blooded tropical animals to climate change. We show that tropical animals may indeed face significant impacts of warming, but that the degree of impact may vary across a species' range. Even at the relatively small scale of the island of Puerto Rico, different populations of a single tropical species may differ greatly in their vulnerability to climate warming.

Image caption: A male Puerto Rican crested anole (Anolis cristatellus). Courtesy of Manuel Leal.

 

Herbivore-induced aspen volatiles temporally regulate two different indirect defences in neighbouring plants

Tao Li, Jarmo K. Holopainen, Harri Kokko, Arja I. Tervahauta and James D. Blande

Rooted in place, plants cannot run away from herbivores, so they have to fight back by deploying various defences. In addition to direct defences, such as production of leaf toxins, plants can also defend themselves against herbivore feeding through the release of volatile chemicals or the secretion of extrafloral nectar that attract and recruit predators, natural enemies of herbivores, and thus serve as an indirect defence. Extrafloral nectar is a sweet liquid produced by nectaries that are found outside the flowers.

A plant can induce defences immediately after the first feeding bout, but may also have enhanced (primed) defences to ward off the second bout. In this case the plant has been primed against a later attack by herbivores. Volatiles released from herbivore-damaged plants have been convincingly demonstrated to induce and/or prime defences in undamaged neighbouring plants. However, it remains largely unknown, particularly in woody plants, whether herbivore-induced volatiles induce and/or prime different indirect defences simultaneously.

We used the woody plant hybrid aspen (Populus tremula × tremuloides) to investigate whether herbivore-induced volatiles induce and/or prime volatile emission and nectar secretion in plant neighbours. Hybrid aspen is known to change the blend of volatiles upon feeding by herbivores, and also has extrafloral nectaries whose presence has been shown to be negatively correlated with leaf damage.

We found that volatiles released from herbivore-damaged plants induced undamaged neighbours to increase extrafloral nectar secretion but not volatile emission. However, upon subsequent attack, plants that had previously been exposed to volatiles from damaged neighbours released significantly more volatiles than plants that had no such prior experience, whereas nectar secretion was not enhanced. This implies that exposure to herbivore-induced volatiles primes undamaged neighbours for a stronger induction of volatile emission but not nectar secretion once they are damaged. Our study provides a key example of how plants temporally coordinate different indirect defences in response to early alarm signals and ensuing actual feeding so as to achieve better protection and more optimal use of resources.

Image caption: Extrafloral nectar droplets on a leaf of hybrid aspen (Populus tremula × tremuloides). Courtesy of Jarmo K. Holopainen.

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