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1.  Are we underestimating the genetic variances of dimorphic traits? 
Ecology and Evolution  2015;5(3):590-597.
Populations often contain discrete classes or morphs (e.g., sexual dimorphisms, wing dimorphisms, trophic dimorphisms) characterized by distinct patterns of trait expression. In quantitative genetic analyses, the different morphs can be considered as different environments within which traits are expressed. Genetic variances and covariances can then be estimated independently for each morph or in a combined analysis. In the latter case, morphs can be considered as separate environments in a bivariate analysis or entered as fixed effects in a univariate analysis. Although a common approach, we demonstrate that the latter produces downwardly biased estimates of additive genetic variance and heritability unless the quantitative genetic architecture of the traits concerned is perfectly correlated between the morphs. This result is derived for four widely used quantitative genetic variance partitioning methods. Given that theory predicts the evolution of genotype-by-environment (morph) interactions as a consequence of selection favoring different trait combinations in each morph, we argue that perfect correlations between the genetic architectures of the different morphs are unlikely. A sampling of the recent literature indicates that the majority of researchers studying traits expressed in different morphs recognize this and do estimate morph-specific quantitative genetic architecture. However, ca. 16% of the studies in our sample utilized only univariate, fixed-effects models. We caution against this approach and recommend that it be used only if supported by evidence that the genetic architectures of the different morphs do not differ.
doi:10.1002/ece3.1361
PMCID: PMC4328764
Animal model; between-sex genetic correlation; offspring-parent covariance; sexual dimorphism; sire and dam variances
2.  Ecology and Evolution 
Ecology and Evolution  2015;5(3):i-iii.
doi:10.1002/ece3.1219
PMCID: PMC4328758
3.  Diversity patterns of ground beetles and understory vegetation in mature, secondary, and plantation forest regions of temperate northern China 
Ecology and Evolution  2015;5(3):531-542.
Plantation and secondary forests form increasingly important components of the global forest cover, but our current knowledge about their potential contribution to biodiversity conservation is limited. We surveyed understory plant and carabid species assemblages at three distinct regions in temperate northeastern China, dominated by mature forest (Changbaishan Nature Reserve, sampled in 2011 and 2012), secondary forest (Dongling Mountain, sampled in 2011 and 2012), and forest plantation habitats (Bashang Plateau, sampled in 2006 and 2007), respectively. The α-diversity of both taxonomic groups was highest in plantation forests of the Bashang Plateau. Beetle α-diversity was lowest, but plant and beetle species turnover peaked in the secondary forests of Dongling Mountain, while habitats in the Changbaishan Nature Reserve showed the lowest turnover rates for both taxa. Changbaishan Nature Reserve harbored the highest proportion of forest specialists. Our results suggest that in temperate regions of northern China, the protected larch plantation forest established over extensive areas might play a considerable role in maintaining a high biodiversity in relation to understory herbaceous plant species and carabid assemblages, which can be seen as indicators of forest disturbance. The high proportion of phytophagous carabids and the rarity of forest specialists reflect the relatively homogenous, immature status of the forest ecosystems on the Bashang Plateau. China's last remaining large old-growth forests like the ones on Changbaishan represent stable, mature ecosystems which require particular conservation attention.
doi:10.1002/ece3.1367
PMCID: PMC4328759
α-Diversity; biodiversity conservation; carabids; herbaceous plants; mature forest; turnover
4.  Quantitative genetics of learning ability and resistance to stress in Drosophila melanogaster 
Ecology and Evolution  2015;5(3):543-556.
Even though laboratory evolution experiments have demonstrated genetic variation for learning ability, we know little about the underlying genetic architecture and genetic relationships with other ecologically relevant traits. With a full diallel cross among twelve inbred lines of Drosophila melanogaster originating from a natural population (0.75 < F < 0.93), we investigated the genetic architecture of olfactory learning ability and compared it to that for another behavioral trait (unconditional preference for odors), as well as three traits quantifying the ability to deal with environmental challenges: egg-to-adult survival and developmental rate on a low-quality food, and resistance to a bacterial pathogen. Substantial additive genetic variation was detected for each trait, highlighting their potential to evolve. Genetic effects contributed more than nongenetic parental effects to variation in traits measured at the adult stage: learning, odorant perception, and resistance to infection. In contrast, the two traits quantifying larval tolerance to low-quality food were more strongly affected by parental effects. We found no evidence for genetic correlations between traits, suggesting that these traits could evolve at least to some degree independently of one another. Finally, inbreeding adversely affected all traits.
doi:10.1002/ece3.1379
PMCID: PMC4328760
Additive genetic variation; diallel crossing; Drosophila melanogaster; genetic correlation; learning
5.  Biomarkers of animal health: integrating nutritional ecology, endocrine ecophysiology, ecoimmunology, and geospatial ecology 
Ecology and Evolution  2015;5(3):557-566.
Diverse biomarkers including stable isotope, hormonal, and ecoimmunological assays are powerful tools to assess animal condition. However, an integrative approach is necessary to provide the context essential to understanding how biomarkers reveal animal health in varied ecological conditions. A barrier to such integration is a general lack of awareness of how shared extraction methods from across fields can provide material from the same animal tissues for diverse biomarker assays. In addition, the use of shared methods for extracting differing tissue fractions can also provide biomarkers for how animal health varies across time. Specifically, no study has explicitly illustrated the depth and breadth of spacial and temporal information that can be derived from coupled biomarker assessments on two easily collected tissues: blood and feathers or hair. This study used integrated measures of glucocorticoids, stable isotopes, and parasite loads in the feathers and blood of fall-migrating Northern saw-whet owls (Aegolius acadicus) to illustrate the wealth of knowledge about animal health and ecology across both time and space. In feathers, we assayed deuterium (δD) isotope and corticosterone (CORT) profiles, while in blood we measured CORT and blood parasite levels. We found that while earlier migrating owls had elevated CORT levels relative to later migrating birds, there was also a disassociation between plasma and feather CORT, and blood parasite loads. These results demonstrate how these tissues integrate time periods from weeks to seasons and reflect energetic demands during differing life stages. Taken together, these findings illustrate the potential for integrating diverse biomarkers to assess interactions between environmental factors and animal health across varied time periods without the necessity of continually recapturing and tracking individuals. Combining biomarkers from diverse research fields into an integrated framework hold great promise for advancing our understanding of environmental effects on animal health.
doi:10.1002/ece3.1360
PMCID: PMC4328761
Bioindicators; birds; glucocorticoids; isoscapes; migration; stable isotopes; stress physiology
6.  Evolutionary dynamics of ecological niche in three Rhinogobio fishes from the upper Yangtze River inferred from morphological traits 
Ecology and Evolution  2015;5(3):567-577.
In the past decades, it has been debated whether ecological niche should be conserved among closely related species (phylogenetic niche conservatism, PNC) or largely divergent (traditional ecological niche theory and ecological speciation) and whether niche specialist and generalist might remain in equilibrium or niche generalist could not appear. In this study, we employed morphological traits to describe ecological niche and test whether different niche dimensions exhibit disparate evolutionary patterns. We conducted our analysis on three Rhinogobio fish species (R. typus,R. cylindricus, and R. ventralis) from the upper Yangtze River, China. Among the 32 measured morphological traits except body length, PCA extracted the first four principal components with their loading scores >1.000. To find the PNC among species, Mantel tests were conducted with the Euclidean distances calculated from the four principal components (representing different niche dimensions) against the pairwise distances calculated from mitochondrial cytochrome b sequence variations. The results showed that the second and the third niche dimension, both related to swimming ability and behavior, exhibited phylogenetic conservatism. Further comparison on niche breadth among these three species revealed that the fourth dimension of R. typus showed the greatest width, indicating that this dimension exhibited niche generalism. In conclusion, our results suggested that different niche dimensions could show different evolutionary dynamic patterns: they may exhibit PNC or not, and some dimensions may evolve generalism.
doi:10.1002/ece3.1386
PMCID: PMC4328762
Ecological niche; generalist; morphological trait; niche difference; phylogenetic niche conservatism; Rhinogobio; specialist; the Yangtze River
7.  Estimating the spatial position of marine mammals based on digital camera recordings 
Ecology and Evolution  2015;5(3):578-589.
Estimating the spatial position of organisms is essential to quantify interactions between the organism and the characteristics of its surroundings, for example, predator–prey interactions, habitat selection, and social associations. Because marine mammals spend most of their time under water and may appear at the surface only briefly, determining their exact geographic location can be challenging. Here, we developed a photogrammetric method to accurately estimate the spatial position of marine mammals or birds at the sea surface. Digital recordings containing landscape features with known geographic coordinates can be used to estimate the distance and bearing of each sighting relative to the observation point. The method can correct for frame rotation, estimates pixel size based on the reference points, and can be applied to scenarios with and without a visible horizon. A set of R functions was written to process the images and obtain accurate geographic coordinates for each sighting. The method is applied to estimate the spatiotemporal fine-scale distribution of harbour porpoises in a tidal inlet. Video recordings of harbour porpoises were made from land, using a standard digital single-lens reflex (DSLR) camera, positioned at a height of 9.59 m above mean sea level. Porpoises were detected up to a distance of ∽3136 m (mean 596 m), with a mean location error of 12 m. The method presented here allows for multiple detections of different individuals within a single video frame and for tracking movements of individuals based on repeated sightings. In comparison with traditional methods, this method only requires a digital camera to provide accurate location estimates. It especially has great potential in regions with ample data on local (a)biotic conditions, to help resolve functional mechanisms underlying habitat selection and other behaviors in marine mammals in coastal areas.
doi:10.1002/ece3.1353
PMCID: PMC4328763
Distance; fine-scale distribution patterns; harbour porpoise; marine mammal; photogrammetric; theodolite; tide; video camera
8.  Do mothers prefer helpers or smaller litters? Birth sex ratio and litter size adjustment in cotton-top tamarins (Saguinus oedipus) 
Ecology and Evolution  2015;5(3):598-606.
Sex allocation theory has been a remarkably productive field in behavioral ecology with empirical evidence regularly supporting quantitative theoretical predictions. Across mammals in general and primates in particular, however, support for the various hypotheses has been more equivocal. Population-level sex ratio biases have often been interpreted as supportive, but evidence for small-scale facultative adjustment has rarely been found. The helper repayment (HR) also named the local resource enhancement (LRE) hypothesis predicts that, in cooperatively breeding species, mothers invest more in the sex which assists with rearing future offspring and that this bias will be more pronounced in mothers who require extra assistance (i.e., due to inexperience or a lack of available alloparents). We tested these hypotheses in captive cotton-top tamarins (Saguinus oedipus) utilizing the international studbook and birth records obtained through a questionnaire from ISIS-registered institutions. Infant sex, litter size, mother's age, parity, and group composition (presence of nonreproductive subordinate males and females) were determined from these records. The HR hypothesis was supported over the entire population, which was significantly biased toward males (the “helpful” sex). We found little support for helper repayment at the individual level, as primiparous females and those in groups without alloparents did not exhibit more extreme tendencies to produce male infants. Primiparous females were, however, more likely to produce singleton litters. Singleton births were more likely to be male, which suggests that there may be an interaction between litter size adjustment and sex allocation. This may be interpreted as supportive of the HR hypothesis, but alternative explanations at both the proximate and ultimate levels are possible. These possibilities warrant further consideration when attempting to understand the ambiguous results of primate sex ratio studies so far.
doi:10.1002/ece3.1396
PMCID: PMC4328765
Helper repayment hypothesis; Saguinus oedipus; sex allocation; sex ratio
9.  America's red gold: multiple lineages of cultivated cochineal in Mexico 
Ecology and Evolution  2015;5(3):607-617.
Cultivated cochineal (Dactylopius coccus) produces carminic acid, a valuable red dye used to color textiles, cosmetics, and food. Extant native D. coccus is largely restricted to two populations in the Mexican and the Andean highlands, although the insect's ultimate center of domestication remains unclear. Moreover, due to Mexican D. coccus cultivation's near demise during the 19th century, the genetic diversity of current cochineal stock is unknown. Through genomic sequencing, we identified two divergent D. coccus populations in highland Mexico: one unique to Mexico and another that was more closely related to extant Andean cochineal. Relic diversity is preserved in the crops of small-scale Mexican cochineal farmers. Conversely, larger-scale commercial producers are cultivating the Andean-like cochineal, which may reflect clandestine 20th century importation.
doi:10.1002/ece3.1398
PMCID: PMC4328766
Cochineal; genomics; Mexico; Peru; phylogeography
10.  How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model 
Ecology and Evolution  2015;5(3):618-633.
It is widely expected that physiological and behavioral stress responses will be integrated within divergent stress-coping styles (SCS) and that these may represent opposite ends of a continuously varying reactive–proactive axis. If such a model is valid, then stress response traits should be repeatable and physiological and behavioral responses should also change in an integrated manner along a major axis of among-individual variation. While there is some evidence of association between endocrine and behavioral stress response traits, few studies incorporate repeated observations of both. To test this model, we use a multivariate, repeated measures approach in a captive-bred population of Xiphophorus birchmanni. We quantify among-individual variation in behavioral stress response to an open field trial (OFT) with simulated predator attack (SPA) and measure waterborne steroid hormone levels (cortisol, 11-ketotestosterone) before and after exposure. Under the mild stress stimulus (OFT), (multivariate) behavioral variation among individuals was consistent with a strong axis of personality (shy–bold) or coping style (reactive–proactive) variation. However, behavioral responses to a moderate stressor (SPA) were less repeatable, and robust statistical support for repeatable endocrine state over the full sampling period was limited to 11-ketotestosterone. Although post hoc analysis suggested cortisol expression was repeatable over short time periods, qualitative relationships between behavior and glucocorticoid levels were counter to our a priori expectations. Thus, while our results clearly show among-individual differences in behavioral and endocrine traits associated with stress response, the correlation structure between these is not consistent with a simple proactive–reactive axis of integrated stress-coping style. Additionally, the low repeatability of cortisol suggests caution is warranted if single observations (or indeed repeat measures over short sampling periods) of glucocorticoid traits are used in ecological or evolutionary studies focussed at the individual level.
doi:10.1002/ece3.1395
PMCID: PMC4328767
11-ketotestosterone; Boldness; cortisol; multivariate behavior; repeatability; waterborne steroid collection
11.  Adaptive plasticity and epigenetic variation in response to warming in an Alpine plant 
Ecology and Evolution  2015;5(3):634-647.
Environmentally induced phenotypic plasticity may be a critical component of response to changing environments. We examined local differentiation and adaptive phenotypic plasticity in response to elevated temperature in half-sib lines collected across an elevation gradient for the alpine herb, Wahlenbergia ceracea. Using Amplified Fragment Length Polymorphism (AFLP), we found low but significant genetic differentiation between low- and high-elevation seedlings, and seedlings originating from low elevations grew faster and showed stronger temperature responses (more plasticity) than those from medium and high elevations. Furthermore, plasticity was more often adaptive for plants of low-elevation origin and maladaptive for plants of high elevation. With methylation sensitive-AFLP (MS-AFLP), we revealed an increase in epigenetic variation in response to temperature in low-elevation seedlings. Although we did not find significant direct correlations between MS-AFLP loci and phenotypes, our results demonstrate that adaptive plasticity in temperature response to warming varies over fine spatial scales and suggest the involvement of epigenetic mechanisms in this response.
doi:10.1002/ece3.1329
PMCID: PMC4328768
Adaptive plasticity; amplified fragment length polymorphism; alpine plants; DNA methylation; epigenetics; global warming
12.  Assessing the phylogeographic history of the montane caddisfly Thremma gallicum using mitochondrial and restriction-site-associated DNA (RAD) markers 
Ecology and Evolution  2015;5(3):648-662.
Repeated Quaternary glaciations have significantly shaped the present distribution and diversity of several European species in aquatic and terrestrial habitats. To study the phylogeography of freshwater invertebrates, patterns of intraspecific variation have been examined primarily using mitochondrial DNA markers that may yield results unrepresentative of the true species history. Here, population genetic parameters were inferred for a montane aquatic caddisfly, Thremma gallicum, by sequencing a 658-bp fragment of the mitochondrial CO1 gene, and 12,514 nuclear RAD loci. T. gallicum has a highly disjunct distribution in southern and central Europe, with known populations in the Cantabrian Mountains, Pyrenees, Massif Central, and Black Forest. Both datasets represented rangewide sampling of T. gallicum. For the CO1 dataset, this included 352 specimens from 26 populations, and for the RAD dataset, 17 specimens from eight populations. We tested 20 competing phylogeographic scenarios using approximate Bayesian computation (ABC) and estimated genetic diversity patterns. Support for phylogeographic scenarios and diversity estimates differed between datasets with the RAD data favouring a southern origin of extant populations and indicating the Cantabrian Mountains and Massif Central populations to represent highly diverse populations as compared with the Pyrenees and Black Forest populations. The CO1 data supported a vicariance scenario (north–south) and yielded inconsistent diversity estimates. Permutation tests suggest that a few hundred polymorphic RAD SNPs are necessary for reliable parameter estimates. Our results highlight the potential of RAD and ABC-based hypothesis testing to complement phylogeographic studies on non-model species.
doi:10.1002/ece3.1366
PMCID: PMC4328769
Biogeography; freshwater ecology; next-generation sequencing; phylogeography; Pleistocene glaciations
13.  Discordance between morphological and molecular species boundaries among Caribbean species of the reef sponge Callyspongia 
Ecology and Evolution  2015;5(3):663-675.
Sponges are among the most species-rich and ecologically important taxa on coral reefs, yet documenting their diversity is difficult due to the simplicity and plasticity of their morphological characters. Genetic attempts to identify species are hampered by the slow rate of mitochondrial sequence evolution characteristic of sponges and some other basal metazoans. Here we determine species boundaries of the Caribbean coral reef sponge genus Callyspongia using a multilocus, model-based approach. Based on sequence data from one mitochondrial (COI), one ribosomal (28S), and two single-copy nuclear protein-coding genes, we found evolutionarily distinct lineages were not concordant with current species designations in Callyspongia. While C. fallax,C. tenerrima, and C. plicifera were reciprocally monophyletic, four taxa with different morphologies (C. armigera,C. longissima,C. eschrichtii, and C. vaginalis) formed a monophyletic group and genetic distances among these taxa overlapped distances within them. A model-based method of species delimitation supported collapsing these four into a single evolutionary lineage. Variation in spicule size among these four taxa was partitioned geographically, not by current species designations, indicating that in Callyspongia, these key taxonomic characters are poor indicators of genetic differentiation. Taken together, our results suggest a complex relationship between morphology and species boundaries in sponges.
doi:10.1002/ece3.1381
PMCID: PMC4328770
Gene tree; Porifera; species delimitation; species tree; spicule
14.  Naturally rare versus newly rare: demographic inferences on two timescales inform conservation of Galápagos giant tortoises 
Ecology and Evolution  2015;5(3):676-694.
Long-term population history can influence the genetic effects of recent bottlenecks. Therefore, for threatened or endangered species, an understanding of the past is relevant when formulating conservation strategies. Levels of variation at neutral markers have been useful for estimating local effective population sizes (Ne) and inferring whether population sizes increased or decreased over time. Furthermore, analyses of genotypic, allelic frequency, and phylogenetic information can potentially be used to separate historical from recent demographic changes. For 15 populations of Galápagos giant tortoises (Chelonoidis sp.), we used 12 microsatellite loci and DNA sequences from the mitochondrial control region and a nuclear intron, to reconstruct demographic history on shallow (past ∽100 generations, ∽2500 years) and deep (pre-Holocene, >10 thousand years ago) timescales. At the deep timescale, three populations showed strong signals of growth, but with different magnitudes and timing, indicating different underlying causes. Furthermore, estimated historical Ne of populations across the archipelago showed no correlation with island age or size, underscoring the complexity of predicting demographic history a priori. At the shallow timescale, all populations carried some signature of a genetic bottleneck, and for 12 populations, point estimates of contemporary Ne were very small (i.e., < 50). On the basis of the comparison of these genetic estimates with published census size data, Ne generally represented ∽0.16 of the census size. However, the variance in this ratio across populations was considerable. Overall, our data suggest that idiosyncratic and geographically localized forces shaped the demographic history of tortoise populations. Furthermore, from a conservation perspective, the separation of demographic events occurring on shallow versus deep timescales permits the identification of naturally rare versus newly rare populations; this distinction should facilitate prioritization of management action.
doi:10.1002/ece3.1388
PMCID: PMC4328771
Conservation; demographic history; Galápagos giant tortoise; genetic diversity; population size
15.  Hierarchical analysis of genetic structure in the habitat-specialist Eastern Sand Darter (Ammocrypta pellucida) 
Ecology and Evolution  2015;5(3):695-708.
Quantifying spatial genetic structure can reveal the relative influences of contemporary and historic factors underlying localized and regional patterns of genetic diversity and gene flow – important considerations for the development of effective conservation efforts. Using 10 polymorphic microsatellite loci, we characterize genetic variation among populations across the range of the Eastern Sand Darter (Ammocrypta pellucida), a small riverine percid that is highly dependent on sandy substrate microhabitats. We tested for fine scale, regional, and historic patterns of genetic structure. As expected, significant differentiation was detected among rivers within drainages and among drainages. At finer scales, an unexpected lack of within-river genetic structure among fragmented sandy microhabitats suggests that stratified dispersal resulting from unstable sand bar habitat degradation (natural and anthropogenic) may preclude substantial genetic differentiation within rivers. Among-drainage genetic structure indicates that postglacial (14 kya) drainage connectivity continues to influence contemporary genetic structure among Eastern Sand Darter populations in southern Ontario. These results provide an unexpected contrast to other benthic riverine fish in the Great Lakes drainage and suggest that habitat-specific fishes, such as the Eastern Sand Darter, can evolve dispersal strategies that overcome fragmented and temporally unstable habitats.
doi:10.1002/ece3.1392
PMCID: PMC4328772
Eastern Sand Darter; fragmented habitat; genetic diversity; genetic structure; stratified dispersal
16.  Sexual segregation in North American elk: the role of density dependence 
Ecology and Evolution  2015;5(3):709-721.
We investigated how density-dependent processes and subsequent variation in nutritional condition of individuals influenced both timing and duration of sexual segregation and selection of resources. During 1999–2001, we experimentally created two population densities of North American elk (Cervus elaphus), a high-density population at 20 elk/km2, and a low-density population at 4 elk/km2 to test hypotheses relative to timing and duration of sexual segregation and variation in selection of resources. We used multi-response permutation procedures to investigate patterns of sexual segregation, and resource selection functions to document differences in selection of resources by individuals in high- and low-density populations during sexual segregation and aggregation. The duration of sexual segregation was 2 months longer in the high-density population and likely was influenced by individuals in poorer nutritional condition, which corresponded with later conception and parturition, than at low density. Males and females in the high-density population overlapped in selection of resources to a greater extent than in the low-density population, probably resulting from density-dependent effects of increased intraspecific competition and lower availability of resources.
doi:10.1002/ece3.1397
PMCID: PMC4328773
Cervus elaphus; density dependence; experimental manipulation; intrasexual competition; North American elk; resource selection; sexual segregation
17.  Metabolic variation in natural populations of wild yeast 
Ecology and Evolution  2015;5(3):722-732.
Ecological diversification depends on the extent of genetic variation and on the pattern of covariation with respect to ecological opportunities. We investigated the pattern of utilization of carbon substrates in wild populations of budding yeast Saccharomyces paradoxus. All isolates grew well on a core diet of about 10 substrates, and most were also able to grow on a much larger ancillary diet comprising most of the 190 substrates we tested. There was substantial genetic variation within each population for some substrates. We found geographical variation of substrate use at continental, regional, and local scales. Isolates from Europe and North America could be distinguished on the basis of the pattern of yield across substrates. Two geographical races at the North American sites also differed in the pattern of substrate utilization. Substrate utilization patterns were also geographically correlated at local spatial scales. Pairwise genetic correlations between substrates were predominantly positive, reflecting overall variation in metabolic performance, but there was a consistent negative correlation between categories of substrates in two cases: between the core diet and the ancillary diet, and between pentose and hexose sugars. Such negative correlations in the utilization of substrate from different categories may indicate either intrinsic physiological trade-offs for the uptake and utilization of substrates from different categories, or the accumulation of conditionally neutral mutations. Divergence in substrate use accompanies genetic divergence at all spatial scales in S. paradoxus and may contribute to race formation and speciation.
doi:10.1002/ece3.1376
PMCID: PMC4328774
Ecological diversification; evolution; genetic variation; metabolic trade-offs; microbial metabolic diversity; Saccharomyces paradoxus
18.  A hierarchical Bayesian model to estimate the unobservable predation rate on sawfly cocoons by small mammals 
Ecology and Evolution  2015;5(3):733-742.
Predation by small mammals has been reported as an important mortality factor for the cocoons of sawfly species. However, it is difficult to provide an accurate estimate of newly spun cocoons and subsequent predation rates by small mammals for several reasons. First, all larvae do not spin cocoons at the same time. Second, cocoons are exposed to small mammal predation immediately after being spun. Third, the cocoons of the current generation are indistinguishable from those of the previous generation. We developed a hierarchical Bayesian model to estimate these values from annual one-time soil sampling datasets. To apply this model to an actual data set, field surveys were conducted in eight stands of larch plantations in central Hokkaido (Japan) from 2009 to 2012. Ten 0.04-m2 soil samples were annually collected from each site in mid-October. The abundance of unopened cocoons (I), cocoons emptied by small-mammal predation (M), and empty cocoons caused by something other than small-mammal predation (H) were determined. The abundance of newly spun cocoons, the predation rate by small mammals before and after cocoon sampling, and the annual rate of empty cocoons that remained were estimated. A posterior predictive check yielded Bayesian P-values of 0.54, 0.48, and 0.07 for I, M, and H, respectively. Estimated predation rates showed a significant positive correlation with the number of trap captures of small mammals. Estimates of the number of newly spun cocoons had a significant positive correlation with defoliation intensity. These results indicate that our model showed an acceptable fit, with reasonable estimates. Our model is expected to be widely applicable to all hymenopteran and lepidopteran insects that spin cocoons in soil.
doi:10.1002/ece3.1394
PMCID: PMC4328775
Apodemus argenteus; Apodemus speciosus; cocoon dynamic models; Myodes rufocanus bedfordiae; predation rate estimation
19.  Detecting a hierarchical genetic population structure: the case study of the Fire Salamander (Salamandra salamandra) in Northern Italy 
Ecology and Evolution  2015;5(3):743-758.
The multistep method here applied in studying the genetic structure of a low dispersal and philopatric species, such as the Fire Salamander Salamandra salamandra, was proved to be effective in identifying the hierarchical structure of populations living in broad-leaved forest ecosystems in Northern Italy. In this study, 477 salamander larvae, collected in 28 sampling populations (SPs) in the Prealpine and in the foothill areas of Northern Italy, were genotyped at 16 specie-specific microsatellites. SPs showed a significant overall genetic variation (Global FST = 0.032, P < 0.001). The genetic population structure was assessed by using STRUCTURE 2.3.4. We found two main genetic groups, one represented by SPs inhabiting the Prealpine belt, which maintain connections with those of the Eastern foothill lowland (PEF), and a second group with the SPs of the Western foothill lowland (WF). The two groups were significantly distinct with a Global FST of 0.010 (P < 0.001). While the first group showed a moderate structure, with only one divergent SP (Global FST = 0.006, P < 0.001), the second group proved more structured being divided in four clusters (Global FST = 0.017, P = 0.058). This genetic population structure should be due to the large conurbations and main roads that separate the WF group from the Prealpine belt and the Eastern foothill lowland. The adopted methods allowed the analysis of the genetic population structure of Fire Salamander from wide to local scale, identifying different degrees of genetic divergence of their populations derived from forest fragmentation induced by urban and infrastructure sprawl.
doi:10.1002/ece3.1335
PMCID: PMC4328776
Amphibians; broad-leaved forests; fragmented population; microsatellites; STRUCTURE software
20.  No species is an island: testing the effects of biotic interactions on models of avian niche occupation 
Ecology and Evolution  2015;5(3):759-768.
Traditionally, the niche of a species is described as a hypothetical 3D space, constituted by well-known biotic interactions (e.g. predation, competition, trophic relationships, resource–consumer interactions, etc.) and various abiotic environmental factors. Species distribution models (SDMs), also called “niche models” and often used to predict wildlife distribution at landscape scale, are typically constructed using abiotic factors with biotic interactions generally been ignored. Here, we compared the goodness of fit of SDMs for red-backed shrike Lanius collurio in farmlands of Western Poland, using both the classical approach (modeled only on environmental variables) and the approach which included also other potentially associated bird species. The potential associations among species were derived from the relevant ecological literature and by a correlation matrix of occurrences. Our findings highlight the importance of including heterospecific interactions in improving our understanding of niche occupation for bird species. We suggest that suite of measures currently used to quantify realized species niches could be improved by also considering the occurrence of certain associated species. Then, an hypothetical “species 1” can use the occurrence of a successfully established individual of “species 2” as indicator or “trace” of the location of available suitable habitat to breed. We hypothesize this kind of biotic interaction as the “heterospecific trace effect” (HTE): an interaction based on the availability and use of “public information” provided by individuals from different species. Finally, we discuss about the incomes of biotic interactions for enhancing the predictive capacities on species distribution models.
doi:10.1002/ece3.1387
PMCID: PMC4328777
Avian niche; biotic interactions; red-backed shrike; species association; species distribution models
21.  Integrated survival analysis using an event-time approach in a Bayesian framework 
Ecology and Evolution  2015;5(3):769-780.
Event-time or continuous-time statistical approaches have been applied throughout the biostatistical literature and have led to numerous scientific advances. However, these techniques have traditionally relied on knowing failure times. This has limited application of these analyses, particularly, within the ecological field where fates of marked animals may be unknown. To address these limitations, we developed an integrated approach within a Bayesian framework to estimate hazard rates in the face of unknown fates. We combine failure/survival times from individuals whose fates are known and times of which are interval-censored with information from those whose fates are unknown, and model the process of detecting animals with unknown fates. This provides the foundation for our integrated model and permits necessary parameter estimation. We provide the Bayesian model, its derivation, and use simulation techniques to investigate the properties and performance of our approach under several scenarios. Lastly, we apply our estimation technique using a piece-wise constant hazard function to investigate the effects of year, age, chick size and sex, sex of the tending adult, and nesting habitat on mortality hazard rates of the endangered mountain plover (Charadrius montanus) chicks. Traditional models were inappropriate for this analysis because fates of some individual chicks were unknown due to failed radio transmitters. Simulations revealed biases of posterior mean estimates were minimal (≤ 4.95%), and posterior distributions behaved as expected with RMSE of the estimates decreasing as sample sizes, detection probability, and survival increased. We determined mortality hazard rates for plover chicks were highest at <5 days old and were lower for chicks with larger birth weights and/or whose nest was within agricultural habitats. Based on its performance, our approach greatly expands the range of problems for which event-time analyses can be used by eliminating the need for having completely known fate data.
doi:10.1002/ece3.1399
PMCID: PMC4328778
Charadrius montanus; continuous time; detection probability; event time; hazard rate; mountain plover; simulation; survival; unknown fate
22.  Evolution of leaf warbler songs (Aves: Phylloscopidae) 
Ecology and Evolution  2015;5(3):781-798.
Songs in passerine birds are important for territory defense and mating. Speciation rates in oscine passerines are so high, due to cultural evolution, that this bird lineage makes up half of the extant bird species. Leaf warblers are a speciose Old-World passerine family of limited morphological differentiation, so that songs are even more important for species delimitation. We took 16 sonographic traits from song recordings of 80 leaf warbler taxa and correlated them with 15 potentially explanatory variables, pairwise, and in linear models. Based on a well-resolved molecular phylogeny of the same taxa, all pairwise correlations were corrected for relatedness with phylogenetically independent contrasts and phylogenetic generalized linear models were used. We found a phylogenetic signal for most song traits, but a strong one only for the duration of the longest and of the shortest element, which are presumably inherited instead of learned. Body size of a leaf warbler species is a constraint on song frequencies independent of phylogeny. At least in this study, habitat density had only marginal impact on song features, which even disappeared through phylogenetic correction. Maybe most leaf warblers avoid the deterioration through sound propagation in dense vegetation by singing from exposed perches. Latitudinal (and longitudinal) extension of the breeding ranges was correlated with most song features, especially verse duration (longer polewards and westwards) and complexity (lower polewards). Climate niche or expansion history might explain these correlations. The number of different element types per verse decreases with elevation, possibly due to fewer resources and congeneric species at higher elevations.
doi:10.1002/ece3.1400
PMCID: PMC4328779
Model of evolution; Phylloscopus; phylogenetic signal; Seicercus; song evolution
23.  On the use of stable oxygen isotope (δ18O) measurements for tracking avian movements in North America 
Ecology and Evolution  2015;5(3):799-806.
Tracking migratory animals has benefitted using measurements of naturally occurring stable isotopes of hydrogen (δ2H) in keratinous tissues such as hair and feathers to link animal origins to continental patterns or isoscapes of δ2H in precipitation. However, for most taxa, much less information exists on the use of stable oxygen isotope ratios (δ18O) despite the fact that δ2H and δ18O are strongly linked in environmental waters through the meteoric relationship and the possibility of using both isotopes to infer greater information on origins and climatic conditions where tissues are grown. A fundamental requirement of using stable isotopes to assign individuals and populations to origins is the development of a rescaling function linking environmental food web signals to the tissue of interest and for birds, this has not been carried out. Here, we derived the relationship between H and O isotopes in known source feathers of 104 individuals representing 11 species of insectivorous passerines sampled across the strong precipitation isoscape of North America. We determined again a strong expected relationship between feather δ2H (δ2Hf) and long-term amount-weighted precipitation δ2H (δ2Hp; r2 = 0.77), but the corresponding relationship between δ18Of and δ18Op was poor (r2 = 0.32) for the same samples. This suggests that δ2H measurements are currently more useful for assignment of insectivorous songbirds to precipitation isoscapes but does not preclude other uses of the δ18Of data. Currently, mechanisms responsible for the decoupling of H and O isotopes in food webs is poorly known, and we advocate a much broader sampling of both isotopes in the same keratinous tissues across precipitation isotope gradients and across taxa to resolve this issue and to increase the power of using water isotopes to track migratory animals.
doi:10.1002/ece3.1383
PMCID: PMC4328780
Assignment; deuterium; isoscapes; oxygen-18; rescaling function; stable isotopes
24.  Limited sampling hampers “big data” estimation of species richness in a tropical biodiversity hotspot 
Ecology and Evolution  2015;5(3):807-820.
Macro-scale species richness studies often use museum specimens as their main source of information. However, such datasets are often strongly biased due to variation in sampling effort in space and time. These biases may strongly affect diversity estimates and may, thereby, obstruct solid inference on the underlying diversity drivers, as well as mislead conservation prioritization. In recent years, this has resulted in an increased focus on developing methods to correct for sampling bias. In this study, we use sample-size-correcting methods to examine patterns of tropical plant diversity in Ecuador, one of the most species-rich and climatically heterogeneous biodiversity hotspots. Species richness estimates were calculated based on 205,735 georeferenced specimens of 15,788 species using the Margalef diversity index, the Chao estimator, the second-order Jackknife and Bootstrapping resampling methods, and Hill numbers and rarefaction. Species richness was heavily correlated with sampling effort, and only rarefaction was able to remove this effect, and we recommend this method for estimation of species richness with “big data” collections.
doi:10.1002/ece3.1405
PMCID: PMC4328781
Ecuador; rarefaction; resampling; richness estimation; sampling effort
25.  Issue Information 
Ecology and Evolution  2015;5(1):i-iii.
doi:10.1002/ece3.1217
PMCID: PMC4298430  PMID: 25628881

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