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1.  Host Use Patterns by the European Woodwasp, Sirex noctilio, in Its Native and Invaded Range 
PLoS ONE  2014;9(3):e90321.
Accelerating introductions of forest insects challenge decision-makers who might or might not respond with surveillance programs, quarantines, eradication efforts, or biological control programs. Comparing ecological controls on indigenous vs. introduced populations could inform responses to new introductions. We studied the European woodwasp, Sirex noctilio, which is not a pest in its native forests, is a serious invasive pest in the southern hemisphere, and now has an uncertain future in North America after its introduction there. Indigenous populations of S. noctilio (in Galicia, Spain) resembled those in New York in that S. noctilio were largely restricted to suppressed trees that were also dying for other reasons, and still only some dying trees showed evidence of S. noctilio: 20–40% and 35–51% in Galicia and New York, respectively. In both areas, P. sylvestris (native to Europe) was the species most likely to have attacks in non-suppressed trees. P. resinosa, native to North America, does not appear dangerously susceptible to S. noctilio. P. radiata, which sustains high damage in the southern hemisphere, is apparently not innately susceptible because in Galicia it was less often used by native S. noctilio than either native pine (P. pinaster and P. sylvestris). Silvicultural practices in Galicia that maintain basal area at 25–40 m2/ha limit S. noctilio abundance. More than 25 species of other xylophagous insects feed on pine in Galicia, but co-occurrences with S. noctilio were infrequent, so strong interspecific competition seemed unlikely. Evidently, S. noctilio in northeastern North America will be more similar to indigenous populations in Europe, where it is not a pest, than to introduced populations in the southern hemisphere, where it is. However, S. noctilio populations could behave differently when they reach forests of the southeastern U.S., where tree species, soils, climate, ecology, management, and landscape configurations of pine stands are different.
PMCID: PMC3968001  PMID: 24675574
2.  Coping with Uncertainty: Woodpecker Finches (Cactospiza pallida) from an Unpredictable Habitat Are More Flexible than Birds from a Stable Habitat 
PLoS ONE  2014;9(3):e91718.
Behavioural flexibility is thought to be a major factor in evolution. It may facilitate the discovery and exploitation of new resources, which in turn may expose populations to novel selective forces and facilitate adaptive radiation. Darwin's finches are a textbook example of adaptive radiation. They are fast learners and show a range of unusual foraging techniques, probably as a result of their flexibility. In this study we aimed to test whether variability of the environment is correlated with flexibility. We compared woodpecker finches from a dry area (hereafter, Arid Zone), where food availability is variable, with individuals from a cloud forest (hereafter, Scalesia zone) where food abundance is stable. As parameters for flexibility, we measured neophilia and neophobia, which are two aspects of reaction to novelty, reversal learning and problem-solving. We found no differences in performance on a problem-solving task but, in line with our prediction, individuals from the Arid Zone were significantly faster reversal learners and more neophilic than their conspecifics from the Scalesia zone. The latter result supports the notion that environmental variability drives flexibility. In contrast to our prediction, Arid Zone birds were even more neophobic than birds from the Scalesia Zone. The latter result could be the consequence of differences in predation pressure between the two vegetation zones.
PMCID: PMC3956741  PMID: 24638107
3.  The Relative Effectiveness of Signaling Systems: Relying on External Items Reduces Signaling Accuracy while Leks Increase Accuracy 
PLoS ONE  2014;9(3):e91725.
Multiple evolutionary phenomena require individual animals to assess conspecifics based on behaviors, morphology, or both. Both behavior and morphology can provide information about individuals and are often used as signals to convey information about quality, motivation, or energetic output. In certain cases, conspecific receivers of this information must rank these signaling individuals based on specific traits. The efficacy of information transfer associated within a signal is likely related to the type of trait used to signal, though few studies have investigated the relative effectiveness of contrasting signaling systems. I present a set of models that represent a large portion of signaling systems and compare them in terms of the ability of receivers to rank signalers accurately. Receivers more accurately assess signalers if the signalers use traits that do not require non-food resources; similarly, receivers more accurately ranked signalers if all the signalers could be observed simultaneously, similar to leks. Surprisingly, I also found that receivers are only slightly better at ranking signaler effort if the effort results in a cumulative structure. This series of findings suggests that receivers may attend to specific traits because the traits provide more information relative to others; and similarly, these results may explain the preponderance of morphological and behavioral display signals.
PMCID: PMC3953539  PMID: 24626221
4.  Diet Quality Limits Summer Growth of Field Vole Populations 
PLoS ONE  2014;9(3):e91113.
Marked variation occurs in both seasonal and multiannual population density peaks of northern European small mammal species, including voles. The availability of dietary proteins is a key factor limiting the population growth of herbivore species. The objective of this study is to investigate the degree to which protein availability influences the growth of increasing vole populations. We hypothesise that the summer growth of folivorous vole populations is positively associated with dietary protein availability. A field experiment was conducted over a summer reproductive period in 18 vegetated enclosures. Populations of field voles (Microtus agrestis) were randomised amongst three treatment groups: 1) food supplementation with ad libitum high protein (30% dry weight) pellets, 2) food supplementation with ad libitum low protein (1% dry weight; both supplemented foods had equivalent energy content) pellets, and 3) control (no food supplementation), n = 6 per treatment. Vole density, survival, demographic attributes and condition indicators were monitored with live-trapping and blood sampling. Highest final vole densities were attained in populations that received high protein supplementation and lowest in low protein populations. Control populations displayed intermediate densities. The survival rate of voles was similar in all treatment groups. The proportion of females, and of those that were pregnant or lactating, was highest in the high protein supplemented populations. This suggests that variation in reproductive, rather than survival rates of voles, accounted for density differences between the treatment groups. We found no clear association between population demography and individual physiological condition. Our results demonstrate that dietary protein availability limits vole population growth during the summer growing season. This suggests that the nutritional quality of forage may be an underestimated source of interannual variation in the density and growth rates of widely fluctuating populations of herbivorous small mammals.
PMCID: PMC3951337  PMID: 24621513
5.  Females tend to prefer genetically similar mates in an island population of house sparrows 
It is often proposed that females should select genetically dissimilar mates to maximize offspring genetic diversity and avoid inbreeding. Several recent studies have provided mixed evidence, however, and in some instances females seem to prefer genetically similar males. A preference for genetically similar mates can be adaptive if outbreeding depression is more harmful than inbreeding depression or if females gain inclusive fitness benefits by mating with close kin. Here, we investigated genetic compatibility and mating patterns in an insular population of house sparrow (Passer domesticus), over a three-year period, using 12 microsatellite markers and one major histocompability complex (MHC) class I gene. Given the small population size and the distance from the mainland, we expected a reduced gene flow in this insular population and we predicted that females would show mating preferences for genetically dissimilar mates.
Contrary to our expectation, we found that offspring were less genetically diverse (multi-locus heterozygosity) than expected under a random mating, suggesting that females tended to mate with genetically similar males. We found high levels of extra-pair paternity, and offspring sired by extra-pair males had a better fledging success than those sired by the social male. Again, unexpectedly, females tended to be more closely related to extra-pair mates than to their social mates. Our results did not depend on the type of genetic marker used, since microsatellites and MHC genes provided similar results, and we found only little evidence for MHC-dependent mating patterns.
These results are in agreement with the idea that mating with genetically similar mates can either avoid the disruption of co-adapted genes or confer a benefit in terms of kin selection.
PMCID: PMC3984696  PMID: 24621140
Sexual selection; Mate choice; Passer domesticus; Major Histocompatibility Complex (MHC); Microsatellites; Extra-pair paternity
6.  Age-Dependent Male Mating Investment in Drosophila pseudoobscura 
PLoS ONE  2014;9(2):e88700.
Male mating investment can strongly influence fitness gained from a mating. Yet, male mating investment often changes with age. Life history theory predicts that mating investment should increase with age, and males should become less discriminatory about their mate as they age. Understanding age-dependent changes in male behavior and their effects on fitness is important for understanding how selection acts in age-structured populations. Although the independent effects of male or female age have been studied in many species, how these interact to influence male mating investment and fitness is less well understood. We mated Drosophila pseudoobscura males of five different age classes (4-, 8-, 11-, 15-, 19-day old) to either young (4-day) or old (11-day) females, and measured copulation duration and early post-mating fecundity. Along with their independent effects, we found a strong interaction between the effects of male and female ages on male mating investment and fitness from individual matings. Male mating investment increased with male age, but this increase was more prominent in matings with young females. Male D. pseudoobscura made smaller investments when mating with old females. The level of such discrimination based on female age, however, also changed with male age. Intermediate aged males were most discriminatory, while the youngest and the oldest males did not discriminate between females of different ages. We also found that larger male mating investments resulted in higher fitness payoffs. Our results show that male and female ages interact to form a complex pattern of age-specific male mating investment and fitness.
PMCID: PMC3929311  PMID: 24586373
7.  Disentangling the Phylogenetic and Ecological Components of Spider Phenotypic Variation 
PLoS ONE  2014;9(2):e89314.
An understanding of how the degree of phylogenetic relatedness influences the ecological similarity among species is crucial to inferring the mechanisms governing the assembly of communities. We evaluated the relative importance of spider phylogenetic relationships and ecological niche (plant morphological variables) to the variation in spider body size and shape by comparing spiders at different scales: (i) between bromeliads and dicot plants (i.e., habitat scale) and (ii) among bromeliads with distinct architectural features (i.e., microhabitat scale). We partitioned the interspecific variation in body size and shape into phylogenetic (that express trait values as expected by phylogenetic relationships among species) and ecological components (that express trait values independent of phylogenetic relationships). At the habitat scale, bromeliad spiders were larger and flatter than spiders associated with the surrounding dicots. At this scale, plant morphology sorted out close related spiders. Our results showed that spider flatness is phylogenetically clustered at the habitat scale, whereas it is phylogenetically overdispersed at the microhabitat scale, although phylogenic signal is present in both scales. Taken together, these results suggest that whereas at the habitat scale selective colonization affect spider body size and shape, at fine scales both selective colonization and adaptive evolution determine spider body shape. By partitioning the phylogenetic and ecological components of phenotypic variation, we were able to disentangle the evolutionary history of distinct spider traits and show that plant architecture plays a role in the evolution of spider body size and shape. We also discussed the relevance in considering multiple scales when studying phylogenetic community structure.
PMCID: PMC3942061  PMID: 24651264
8.  Life-History Consequences of Chronic Nutritional Stress in an Outbreaking Insect Defoliator 
PLoS ONE  2014;9(2):e88039.
Food shortage is a common situation in nature but little is known about the strategies animals use to overcome it. This lack of knowledge is especially true for outbreaking insects, which commonly experience nutritional stress for several successive generations when they reach high population densities. The aim of this study is to evaluate the life history consequences of chronic nutritional stress in the outbreaking moth Choristoneura fumiferana. Larvae were reared on two different artificial diets that emulate nutritional conditions larvae face during their natural population density cycle (low and medium quality artificial diets). After four generations, a subset of larvae was fed on the same diet as their parents, and another on the opposite diet. We explored larval life-history strategies to cope with nutritional stress, its associated costs and the influence of nutritional conditions experienced in the parental generation. We found no evidence of nutritional stress in the parental generation increasing offspring ability to feed on low quality diet, but the contrary: compared to offspring from parents that were fed a medium quality diet, larvae from parents fed a low quality diet had increased mortality, reduced growth rate and reduced female reproductive output. Our results support a simple stress hypothesis because the negative effects of malnutrition accumulated over successive generations. Density-dependent deterioration in plant quality is thought to be an important factor governing the population dynamics of outbreaking insects and we hypothesize that chronic nutritional stress can be a driver of outbreak declines of C. fumiferana, and of forest insects in general.
PMCID: PMC3914887  PMID: 24505368
9.  Interspecific Aggressive Behaviour of Invasive Pumpkinseed Lepomis gibbosus in Iberian Fresh Waters 
PLoS ONE  2014;9(2):e88038.
Pumpkinseed Lepomis gibbosus (L.) are successful invaders in Europe, where this species exerts multiple ecological effects, mainly through trophic interactions. Behavioural interference represents a potential impact for native fauna and this is of particular conservation concern in the Iberian Peninsula because of the highly valuable endemic fauna inhabiting streams of this region. However, aggressive interactions have not previously been examined under natural conditions in Iberian fresh waters. To address this gap in knowledge, the aim of the present study was to assess the effect of pumpkinseed aggression on endemic fauna of an Iberian stream, the River Bullaque (central Spain). In September 2009, we analysed the aggression and environmental contexts of these behavioural interactions by snorkelling: aggressor size, aggression type, shoal size, previous activity to aggression, recipient species, response to aggression, microhabitat structure and prey availability. Small pumpkinseed displayed more threat and fewer pursuit behaviours relative to medium and large individuals, reflecting an ontogenetic behavioural shift from low to high aggression intensity. Small aggressors came from large shoals, with bottom feeding being the most frequently observed activity prior to an aggressive interaction; whereas large pumpkinseed were less gregarious and they were mostly ambulating within the water column prior to aggression. Recipient species of aggression included non-native crayfish and fishes, and more importantly, endemic fishes and frogs. Retreat was the most common response to aggression, irrespective of aggressor size. Small pumpkinseed displayed aggressive behaviours over coarse substrata containing elevated macrobenthos biomass; whereas aggression by large individuals was observed in deeper waters. These findings suggest that small and large pumpkinseed exert a high impact on other stream residents through aggression in competition for food and territory defence, respectively. This study highlights the usefulness of direct observations in the wild for assessing the effects of behavioural interference of invasive fishes on Iberian aquatic communities.
PMCID: PMC3914894  PMID: 24505367
10.  Plastic and the Nest Entanglement of Urban and Agricultural Crows 
PLoS ONE  2014;9(1):e88006.
Much attention has been paid to the impacts of plastics and other debris on marine organisms, but the effects of plastic on terrestrial organisms have been largely ignored. Detrimental effects of terrestrial plastic could be most pronounced in intensively human-modified landscapes (e.g., urban and agricultural areas), which are a source of much anthropogenic debris. Here, we examine the occurrence, types, landscape associations, and consequences of anthropogenic nest material in the American crow (Corvus brachyrhynchos), a North American species that breeds in both urban and agricultural landscapes. We monitored 195 nestlings in 106 nests across an urban and agricultural gradient in the Sacramento Valley, California, USA. We found that 85.2% of crow nests contained anthropogenic material, and 11 of 195 nestlings (5.6%) were entangled in their nests. The length of the material was greater in nests in agricultural territories than in urban territories, and the odds of entanglement increased 7.55 times for each meter of anthropogenic material in the nest. Fledging success was significantly lower for entangled than for unentangled nestlings. In all environments, particularly urban, agricultural, and marine, careful disposal of potential hazards (string, packing and hay bale twine, balloon ribbon, wire, fishing line) could reduce the occurrence of entanglement of nestling birds.
PMCID: PMC3909286  PMID: 24498238
11.  Disrupting Immune Regulation Incurs Transient Costs in Male Reproductive Function 
PLoS ONE  2014;9(1):e84606.
Immune protection against pathogenic organisms has been shown to incur costs. Previous studies investigating the cost of immunity have mostly focused on the metabolic requirements of immune maintenance and activation. In addition to these metabolic costs, the immune system can induce damage to the host if the immune response is mis-targeted or over-expressed. Given its non-specific nature, an over-expressed inflammatory response is often associated with substantial damage for the host. Here, we investigated the cost of an over-expressed inflammatory response in the reproductive function of male mice.
Methodology/Principal Findings
We experimentally blocked the receptors of an anti-inflammatory cytokine (IL-10) in male mice exposed to a mild inflammatory challenge, with each treatment having an appropriate control group. The experiment was conducted on two age classes, young (3 month old) and old (15 month old) mice, to assess any age-related difference in the cost of a disrupted immune regulation. We found that the concomitant exposure to an inflammatory insult and the blockade of IL-10 induced a reduction in testis mass, compared to the three other groups. The frequency of abnormal sperm morphology was also higher in the group of mice exposed to the inflammatory challenge but did not depend on the blockade of the IL-10.
Our results provide evidence that immune regulation confers protection against the risk of inflammation-induced infertility during infection. They also suggest that disruption of the effectors involved in the regulation of the inflammatory response can have serious fitness consequences even under mild inflammatory insult and benign environmental conditions.
PMCID: PMC3882243  PMID: 24400103
12.  The PHA Test as an Indicator of Phagocytic Activity in a Passerine Bird 
PLoS ONE  2013;8(12):e84108.
Several techniques in ecological immunology have been used to assess bird immunocompetence thus providing useful information to understand the contribution of the immunological system in life-history decisions. The phytohaemagglutinin (PHA)-skin test has been the most widely employed technique being interpreted as the sole result of T lymphocytes proliferation and hence used to evaluate acquired immunological capacity. However, the presence of high numbers of phagocytic cells in the swelling point has cast some doubt about such an assumption. To address this issue, we collected blood from 14 days-old nestlings of spotless starling (Sturnus unicolor), administered subcutaneous PHA immediately after and then measured the swelling response 24 hours later. Differential counts of white blood cells suggested that an intense development of acquired immunological defences was taking place. The phagocytic activity of both heterophiles and monocytes was also very intense as it was the swelling response. Moreover, our results show, for the first time in birds, a positive relationship between the phagocytic activity of both kinds of cells and the swelling response. This broadens the significance of the PHA test from reflecting T lymphocytes proliferation -as previously proposed but still undetermined in vivo- to evaluate phagocytosis as well. In other words, our data suggest that the PHA swelling response may not be considered as the only consequence of processes of specific and induced immunity –T lymphocytes proliferation- but also of constitutive and nonspecific immunity –heterophiles and monocytes phagocytosis. We propose the extensive use of PHA-skin test as an optimal technique to assess immunocompetence.
PMCID: PMC3877195  PMID: 24391896
13.  Food Selectivity and Diet Switch Can Explain the Slow Feeding of Herbivorous Coral-Reef Fishes during the Morning 
PLoS ONE  2013;8(12):e82391.
Most herbivorous coral-reef fishes feed slower in the morning than in the afternoon. Given the typical scarcity of algae in coral reefs, this behavior seems maladaptive. Here we suggest that the fishes' slow feeding during the morning is an outcome of highly selective feeding on scarcely found green algae. The rarity of the food requires longer search time and extended swimming tracks, resulting in lower bite rates. According to our findings by noon the fish seem to stop their search and switch to indiscriminative consumption of benthic algae, resulting in apparent higher feeding rates. The abundance of the rare preferable algae gradually declines from morning to noon and seems to reach its lowest levels around the switch time. Using in situ experiments we found that the feeding pattern is flexible, with the fish exhibiting fast feeding rates when presented with ample supply of preferable algae, regardless of the time of day. Analyses of the fish's esophagus content corroborated our conclusion that their feeding was highly selective in the morning and non-selective in the afternoon. Modeling of the fishes' behavior predicted that the fish should perform a diel diet shift when the preferred food is relatively rare, a situation common in most coral reefs found in a warm, oligotrophic ocean.
PMCID: PMC3866113  PMID: 24358178
14.  Personality Variation in Little Brown Bats 
PLoS ONE  2013;8(11):e80230.
Animal personality or temperament refers to individual differences in behaviour that are repeatable over time and across contexts. Personality has been linked to life-history traits, energetic traits and fitness, with implications for the evolution of behaviour. Personality has been quantified for a range of taxa (e.g., fish, songbirds, small mammals) but, so far, there has been little work on personality in bats, despite their diversity and potential as a model taxon for comparative studies. We used a novel environment test to quantify personality in little brown bats (Myotis lucifugus) and assess the short-term repeatability of a range of behaviours. We tested the hypothesis that development influences values of personality traits and predicted that trait values associated with activity would increase between newly volant, pre-weaning young-of-the-year (YOY) and more mature, self-sufficient YOY. We identified personality dimensions that were consistent with past studies of other taxa and found that these traits were repeatable over a 24-hour period. Consistent with our prediction, older YOY captured at a fall swarming site prior to hibernation had higher activity scores than younger YOY bats captured at a maternity colony, suggesting that personality traits vary as development progresses in YOY bats. Thus, we found evidence of short-term consistency of personality within individuals but with the potential for temporal flexibility of traits, depending on age.
PMCID: PMC3842255  PMID: 24312205
15.  Altering an extended phenotype reduces intraspecific male aggression and can maintain diversity in cichlid fish 
PeerJ  2013;1:e209.
Reduced male aggression towards different phenotypes generating negative frequency-dependent intrasexual selection has been suggested as a mechanism to facilitate the invasion and maintenance of novel phenotypes in a population. To date, the best empirical evidence for the phenomenon has been provided by laboratory studies on cichlid fish with different colour polymorphisms. Here we experimentally tested the hypothesis in a natural population of Lake Malawi cichlid fish, in which males build sand-castles (bowers) to attract females during seasonal leks. We predicted that if bower shape plays an important role in male aggressive interactions, aggression among conspecific males should decrease when their bower shape is altered. Accordingly, we allocated randomly chosen bowers in a Nyassachromis cf. microcephalus lek into three treatments: control, manipulated to a different shape, and simulated manipulation. We then measured male behaviours and bower shape before and after these treatments. We found that once bower shape was altered, males were involved in significantly fewer aggressive interactions with conspecific males than before manipulation. Mating success was not affected. Our results support the idea that an extended phenotype, such as bower shape, can be important in maintaining polymorphic populations. Specifically, reduced male conspecific aggression towards males with different extended phenotypes (here, bower shapes) may cause negative frequency-dependent selection, allowing the invasion and establishment of a new phenotype (bower builder). This could help our understanding of mechanisms of diversification within populations, and in particular, the overall diversification of bower shapes within Lake Malawi cichlids.
PMCID: PMC3845871  PMID: 24349896
Male aggression; Extended phenotype; Negative frequency-dependent intrasexual selection; Female preference; Haplochromine cichlid; Lake Malawi; Bower
16.  Experimental Manipulation of Melanism Demonstrates the Plasticity of Preferred Temperature in an Agricultural Pest (Phaulacridium vittatum) 
PLoS ONE  2013;8(11):e80243.
Phenotypic plasticity is a key trait of successful pest species, and may increase the ability to cope with higher, more variable temperatures under climate change. We investigate the plasticity of preferred temperature in a widespread agricultural pest, the wingless grasshopper (Phaulacridium vittatum). Preferred temperature is a measure of thermoregulatory behaviour through habitat selection. It is influenced by melanism, which affects body temperature by determining the amount of radiation absorbed by the body. First we demonstrate that body temperature and preferred temperature in P. vittatum is influenced by melanism, by comparing the preferred temperature of the colour morphs in laboratory thermal gradients and field body temperatures in natural populations. We then test whether preferred temperature changes in response to changes in body temperature, by determining preferred temperature before and after manipulation of melanism by painting. When melanism was manipulated experimentally in live grasshoppers, preferred temperature changed to reflect the thermal qualities of the new colour. The preferred temperature of light grasshoppers increased after they were painted black, and decreased after being painted white. Similarly, dark individuals that were painted white behaved like a light individual, maintaining a lower body temperature. Preferred temperature in P.vittatum is a plastic thermoregulatory response to ambient temperature, mediated by the influence of melanism on body temperature.
PMCID: PMC3819283  PMID: 24223223
17.  Size and shape in the evolution of ant worker morphology 
PeerJ  2013;1:e205.
Morphological evolution in ants has been traditionally thought as being strongly influenced by selection for colony ergonomic efficiency. Although many studies have focused on the evolution of social characteristics in ants, little is known about the evolution of worker morphology at a macroevolutionary scale. In this study, we investigate the tempo and mode of the evolution of worker morphology, focusing on changes in size and shape. Our datasets included a large sample of species from different ant genera, as well as variation within the hyperdiverse genus Pheidole, for a total of 1650 measurements. The rate of size evolution was at least five times faster than the rate of shape evolution. The fit of alternative models of morphological evolution indicated statistically significant phylogenetic signal in both size and shape and in all datasets. Finally, tests of rate heterogeneity in phenotypic evolution among lineages identified several shifts in rates of evolution in both datasets, although the timing of shifts in size and shape was usually not concordant.
PMCID: PMC3828632  PMID: 24255818
Lines of least resistance; Allometry; Caste; Morphological innovation
18.  Increase in Male Reproductive Success and Female Reproductive Investment in Invasive Populations of the Harlequin Ladybird Harmonia axyridis 
PLoS ONE  2013;8(10):e77083.
Reproductive strategy affects population dynamics and genetic parameters that can, in turn, affect evolutionary processes during the course of biological invasion. Life-history traits associated with reproductive strategy are therefore potentially good candidates for rapid evolutionary shifts during invasions. In a series of mating trials, we examined mixed groups of four males from invasive and native populations of the harlequin ladybird Harmonia axyridis mating freely during 48 hours with one female of either type. We recorded the identity of the first male to copulate and after the 48 h-period, we examined female fecundity and share of paternity, using molecular markers. We found that invasive populations have a different profile of male and female reproductive output. Males from invasive populations are more likely to mate first and gain a higher proportion of offspring with both invasive and native females. Females from invasive populations reproduce sooner, lay more eggs, and have offspring sired by a larger number of fathers than females from native populations. We found no evidence of direct inbreeding avoidance behaviour in both invasive and native females. This study highlights the importance of investigating evolutionary changes in reproductive strategy and associated traits during biological invasions.
PMCID: PMC3799855  PMID: 24204741
19.  Do Major Roads Reduce Gene Flow in Urban Bird Populations? 
PLoS ONE  2013;8(10):e77026.
Although the negative effects of roads on the genetics of animal populations have been extensively reported, the question of whether roads reduce gene flow in volant, urban bird populations has so far not been addressed. In this study, we assess whether highways decreased gene flow and genetic variation in a small passerine bird, the tree sparrow (Passer montanus).
We assessed genetic differences among tree sparrows (Passer montanus) sampled at 19 sites within Beijing Municipality, China, using 7 DNA microsatellites as genetic markers.
AMOVA showed that genetic variation between sites, between urban and rural populations, and between opposite sides of the same highway, were very weak. Mantel tests on all samples, and on urban samples only, indicated that the age and number of highways, and the number of ordinary roads, were uncorrelated with genetic differences (FST) among tree sparrows from different urban sites. Birds sampled at urban sites had similar levels of genetic diversity to those at rural sites. There was, however, evidence of some weak genetic structure between urban sites. Firstly, there were significant genetic differences (FST) between birds from opposite sides of the same highway, but no significant FST values between those from sites that were not separated by highways. Secondly, birds from eleven urban sites had loci that significantly deviated from the Hardy–Weinberg equilibrium but no such deviation was found in birds from rural sites.
We cannot, therefore, conclusively reject the hypothesis that highways have no effect on the gene flow of tree sparrow populations. Furthermore, since the significance of these results may increase with time, we suggested that research on the influence of highways on gene flow in urban bird populations needs to be conducted over several decades.
PMCID: PMC3800058  PMID: 24204724
20.  Growth but Not Photosynthesis Response of a Host Plant to Infection by a Holoparasitic Plant Depends on Nitrogen Supply 
PLoS ONE  2013;8(10):e75555.
Parasitic plants can adversely influence the growth of their hosts by removing resources and by affecting photosynthesis. Such negative effects depend on resource availability. However, at varied resource levels, to what extent the negative effects on growth are attributed to the effects on photosynthesis has not been well elucidated. Here, we examined the influence of nitrogen supply on the growth and photosynthesis responses of the host plant Mikania micrantha to infection by the holoparasite Cuscuta campestris by focusing on the interaction of nitrogen and infection. Mikania micrantha plants fertilized at 0.2, 1 and 5 mM nitrate were grown with and without C. campestris infection. We observed that the infection significantly reduced M. micrantha growth at each nitrate fertilization and more severely at low than at high nitrate. Such alleviation at high nitrate was largely attributed to a stronger influence of infection on root biomass at low than at high nitrate fertilization. However, although C. campestris altered allometry and inhibited host photosynthesis, the magnitude of the effects was independent of nitrate fertilizations. The infection reduced light saturation point, net photosynthesis at saturating irradiances, apparent quantum yield, CO2 saturated rate of photosynthesis, carboxylation efficiency, the maximum carboxylation rate of Rubisco, and maximum light-saturated rate of electron transport, and increased light compensation point in host leaves similarly across nitrate levels, corresponding to a similar magnitude of negative effects of the parasite on host leaf soluble protein and Rubisco concentrations, photosynthetic nitrogen use efficiency and stomatal conductance across nitrate concentrations. Thus, the more severe inhibition in host growth at low than at high nitrate supplies cannot be attributed to a greater parasite-induced reduction in host photosynthesis, but the result of a higher proportion of host resources transferred to the parasite at low than at high nitrate levels.
PMCID: PMC3792126  PMID: 24116055
21.  Selective Pressure along a Latitudinal Gradient Affects Subindividual Variation in Plants 
PLoS ONE  2013;8(9):e74356.
Individual plants produce repeated structures such as leaves, flowers or fruits, which, although belonging to the same genotype, are not phenotypically identical. Such subindividual variation reflects the potential of individual genotypes to vary with micro-environmental conditions. Furthermore, variation in organ traits imposes costs to foraging animals such as time, energy and increased predation risk. Therefore, animals that interact with plants may respond to this variation and affect plant fitness. Thus, phenotypic variation within an individual plant could be, in part, an adaptive trait. Here we investigated this idea and we found that subindividual variation of fruit size of Crataegus monogyna, in different populations throughout the latitudinal gradient in Europe, was explained at some extent by the selective pressures exerted by seed-dispersing birds. These findings support the hypothesis that within-individual variation in plants is an adaptive trait selected by interacting animals which may have important implications for plant evolution.
PMCID: PMC3778006  PMID: 24069297
22.  Preferred Habitat of Breeding Birds May Be Compromised by Climate Change: Unexpected Effects of an Exceptionally Cold, Wet Spring 
PLoS ONE  2013;8(9):e75536.
Previous studies of the consequences for breeding birds of climate change have explored how their populations may respond to increasing temperatures. However, few have considered the likely outcome of predicted extreme conditions and the relative vulnerability of populations in different habitats. Here, we compare phenology and breeding success in great tits and blue tits over a 10 year period, including the extremely harsh conditions during spring 2012, at three sites in eastern England – mixed deciduous woodland, riparian and urban habitat. Production, measured as brood biomass, was significantly lower in 2012 compared with the previous 9 years, with the decrease in productivity relatively greatest in woodland habitat. Production was related to hatch delay, i.e. birds not initiating incubation immediately after clutch completion, which was more common in 2012 than in previous years. The best predictor of hatch delay was daytime temperature (not nighttime minimum temperature) and rainfall, which convincingly reflected low growth and activity of caterpillar prey. We found that birds breeding in riparian and urban habitats were less vulnerable to the extremes of weather than those breeding in mixed deciduous woodland.
PMCID: PMC3776768  PMID: 24058694
23.  Microgeographic maladaptive performance and deme depression in response to roads and runoff 
PeerJ  2013;1:e163.
Despite theoretical understanding and empirical detection of local adaptation in natural environments, our knowledge of such divergence in fragmented habitats remains limited, especially in the context of microgeographic spatial scales and contemporary time scales. I used a combination of reciprocal transplant and common garden exposure experiments to evaluate potential microgeographic divergence in a pool-breeding amphibian occupying a landscape fragmented by roads. As indicated by reduced rates of survival and increased rates of malformation, I found evidence for maladaptation in road adjacent populations. This response is in direct counterpoint to recently described local adaption by a cohabiting species of amphibian. These results suggest that while divergence might commonly follow habitat modification, the direction of its outcome cannot be generalized even in identical habitats. Further, maladaptive responses can be associated with a more generalized depression effect that transcends the local environment. Alongside recent reports, these results suggest that maladaptive responses may be an emerging consequence of human-induced environmental change. Thus future studies should carefully consider the population unit as a key level for inference.
PMCID: PMC3792186  PMID: 24109548
Microgeographic differentiation; Adaptation and maladaptation; Contemporary evolution; Road salt; Conservation; Roads and runoff
24.  Spatial and Temporal Variation in Heterophil-to-Lymphocyte Ratios of Nestling Passerine Birds: Comparison of Blue Tits and Great Tits 
PLoS ONE  2013;8(9):e74226.
Environmental factors affecting trophic conditions act as stressors on nestling altricial birds. Access of parental birds to a sufficient supply of food in a limited period of the nestling stage differ in time and space, depending on nesting habitat, prey density and weather conditions. Heterophil-to-lymphocyte ratio (H/L) is considered as a reliable indicator of prolonged stress reaction in birds. In this study we examine if variation in H/L shows consistent spatio-temporal patterns in nestlings of two parids, blue tit Cyanistes caeruleus and great tit Parus major. We found that blue tit nestlings had on average higher H/L than great tit nestlings, which corresponds with the ecological sensitivity of these species. In both species H/L was higher in a poor parkland habitat than in a high quality forest habitat. In nestling blue tits, higher H/L values occurred in years characterized by more extreme weather conditions and worse caterpillar availability. Such consistent patterns of variation in the H/L ratio of nestling blue tits and great tits suggest that, when age-dependent effects are controlled, the ratio can be used as an indicator of physiological stress that is generated by food-related stressors differing in space and time. In particular, elevated H/L ratios are indicative of human-induced changes in the structure of breeding habitats.
PMCID: PMC3774732  PMID: 24066123
25.  A Test for Pre-Adapted Phenotypic Plasticity in the Invasive Tree Acer negundo L. 
PLoS ONE  2013;8(9):e74239.
Phenotypic plasticity is a key mechanism associated with the spread of exotic plants and previous studies have found that invasive species are generally more plastic than co-occurring species. Comparatively, the evolution of phenotypic plasticity in plant invasion has received less attention, and in particular, the genetic basis of plasticity is largely unexamined. Native from North America, Acer negundo L. is aggressively impacting the riparian forests of southern and eastern Europe thanks to higher plasticity relative to co-occurring native species. We therefore tested here whether invasive populations have evolved increased plasticity since introduction. The performance of 1152 seedlings from 8 native and 8 invasive populations was compared in response to nutrient availability. Irrespective of nutrients, invasive populations had higher growth and greater allocation to above-ground biomass relative to their native conspecifics. More importantly, invasive genotypes did not show increased plasticity in any of the 20 traits examined. This result suggests that the high magnitude of plasticity to nutrient variation of invasive seedlings might be pre-adapted in the native range. Invasiveness of A. negundo could be explained by higher mean values of traits due to genetic differentiation rather than by evolution of increased plasticity.
PMCID: PMC3767822  PMID: 24040212

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