Abstract View

The Genetic Basis of White Tigers
Xiao Xu, Gui-Xin Dong, Xue-Song Hu, Lin Miao, Xue-Li Zhang, De-Lu Zhang, Han-Dong Yang, Tian-You Zhang, Zheng-Ting Zou, Ting-Ting Zhang, Yan Zhuang, Jong Bhak, Yun Sung Cho, Wen-Tao Dai, Tai-Jiao Jiang, Can Xie, Ruiqiang Li, Shu-Jin Luo
Current Biology – 23 May 2013

The white tiger, an elusive Bengal tiger (Panthera tigris tigris) variant with white fur and dark stripes, has fascinated humans for centuries ever since its discovery in the jungles of India [1]. Many white tigers in captivity are inbred in order to maintain this autosomal recessive trait [2,3,4,5] and consequently suffer some health problems, leading to the controversial speculation that the white tiger mutation is perhaps a genetic defect [6]. However, the genetic basis of this phenotype remains unknown. Here, we conducted genome-wide association mapping with restriction-site-associated DNA sequencing (RAD-seq) in a pedigree of 16 captive tigers segregating at the putative white locus, followed by whole-genome sequencing (WGS) of the three parents. Validation in 130 unrelated tigers identified the causative mutation to be an amino acid change (A477V) in the transporter protein SLC45A2. Three-dimensional homology modeling suggests that the substitution may partially block the transporter channel cavity and thus affect melanogenesis. We demonstrate the feasibility of combining RAD-seq and WGS to rapidly map exotic variants in nonmodel organisms. Our results identify the basis of the longstanding white tiger mystery as the same gene underlying color variation in human, horse, and chicken and highlight its significance as part of the species’ natural polymorphism that is viable in the wild.

White, T. A., Perkins, S. E., Heckel, G. and Searle, J. B. (2013), Adaptive evolution during an ongoing range expansion: the invasive bank vole (Myodes glareolus) in Ireland. Molecular Ecology. doi: 10.1111/mec.12343
Range expansions are extremely common, but have only recently begun to attract attention in terms of their genetic consequences. As populations expand, demes at the wave front experience strong genetic drift, which is expected to reduce genetic diversity and potentially cause ‘allele surfing’, where alleles may become fixed over a wide geographical area even if their effects are deleterious. Previous simulation models show that range expansions can generate very strong selective gradients on dispersal, reproduction, competition and immunity. To investigate the effects of range expansion on genetic diversity and adaptation, we studied the population genomics of the bank vole (Myodes glareolus) in Ireland. The bank vole was likely introduced in the late 1920s and is expanding its range at a rate of ~2.5 km/year. Using genotyping-by-sequencing, we genotyped 281 bank voles at 5979 SNP loci. Fourteen sample sites were arranged in three transects running from the introduction site to the wave front of the expansion. We found significant declines in genetic diversity along all three transects. However, there was no evidence that sites at the wave front had accumulated more deleterious mutations. We looked for outlier loci with strong correlations between allele frequency and distance from the introduction site, where the direction of correlation was the same in all three transects. Amongst these outliers, we found significant enrichment for genic SNPs, suggesting the action of selection. Candidates for selection included several genes with immunological functions and several genes that could influence behaviour.

Velo-Antón, G., Parra, J. L., Parra-Olea, G. and Zamudio, K. R. (2013), Tracking climate change in a dispersal-limited species: reduced spatial and genetic connectivity in a montane salamander. Molecular Ecology. doi: 10.1111/mec.12310
Tropical montane taxa are often locally adapted to very specific climatic conditions, contributing to their lower dispersal potential across complex landscapes. Climate and landscape features in montane regions affect population genetic structure in predictable ways, yet few empirical studies quantify the effects of both factors in shaping genetic structure of montane-adapted taxa. Here, we considered temporal and spatial variability in climate to explain contemporary genetic differentiation between populations of the montane salamander, Pseudoeurycea leprosa. Specifically, we used ecological niche modelling (ENM) and measured spatial connectivity and gene flow (using both mtDNA and microsatellite markers) across extant populations of P. leprosa in the Trans-Mexican Volcanic Belt (TVB). Our results indicate significant spatial and genetic isolation among populations, but we cannot distinguish between isolation by distance over time or current landscape barriers as mechanisms shaping population genetic divergences. Combining ecological niche modelling, spatial connectivity analyses, and historical and contemporary genetic signatures from different classes of genetic markers allows for inference of historical evolutionary processes and predictions of the impacts future climate change will have on the genetic diversity of montane taxa with low dispersal rates. Pseudoeurycea leprosa is one montane species among many endemic to this region and thus is a case study for the continued persistence of spatially and genetically isolated populations in the highly biodiverse TVB of central Mexico.

Voelker, G., Bowie, R. C. K. and Klicka, J. (2013), Gene trees, species trees and Earth history combine to shed light on the evolution of migration in a model avian system. Molecular Ecology. doi: 10.1111/mec.12305
The evolution of migration in birds has fascinated biologists for centuries. In this study, we performed phylogenetic-based analyses of Catharus thrushes, a model genus in the study of avian migration, and their close relatives. For these analyses, we used both mitochondrial and nuclear genes, and the resulting phylogenies were used to trace migratory traits and biogeographic patterns. Our results provide the first robust assessment of relationships within Catharus and relatives and indicate that both mitochondrial and autosomal genes contribute to overall support of the phylogeny. Measures of phylogenetic informativeness indicated that mitochondrial genes provided more signal within Catharus than did nuclear genes, whereas nuclear loci provided more signal for relationships between Catharus and close relatives than did mitochondrial genes. Insertion and deletion events also contributed important support across the phylogeny. Across all taxa included in the study, and for Catharus, possession of long-distance migration is reconstructed as the ancestral condition, and a North American (north of Mexico) ancestral area is inferred. Within Catharus, sedentary behaviour evolved after the first speciation event in the genus and is geographically and temporally correlated with Central American distributions and the final closure of the Central American Seaway. Migratory behaviour subsequently evolved twice in Catharus and is geographically and temporally correlated with a recolonization of North America in the late Pleistocene. By temporally linking speciation events with changes in migratory condition and events in Earth history, we are able to show support for several competing hypotheses relating to the geographic origin of migration.

Yamato Tsuji, Goro Hanya, Cyril C. Grueter
Feeding strategies of primates in temperate and alpine forests: comparison of Asian macaques and colobines
Primates, May 2013

We analyzed regional variation in the diets of two primate clades, Asian macaques and colobines, whose distributions include temperate–alpine forests. We addressed feeding strategies that enabled them to adapt to harsh environments characterized by relatively low mean temperatures and strong seasonality in both temperature and food availability. Macaques in tropical–lowland forests feed mainly on fruit and animal matter whereas populations in temperate–alpine forests feed more on foliage and on such items as bark and fungi. In comparison, colobines in tropical–lowland forests feed more on fruit and foliage whereas populations in temperate–alpine forests feed less on flowers and more on lichens. Annual precipitation and mean temperature, both of which reflect primary production, had the most significant effects on the feeding behavior of the macaques, whereas only mean temperature had a significant effect on that of colobines. We found two behavioral strategies used by both clades to cope with severe environmental conditions in temperate–alpine forests—shifting to other food items and adjusting feeding plasticity for fruit and foliage. Macaques responded to latitudinal changes by use of both strategies whereas the colobines adapted by using the latter only. By contrast, changes in altitude resulted in the macaques’ using the latter strategy and colobines’ using both. The different current distributions of Asian macaques and colobines could be attributed to differences in their feeding strategies originating in their digestive systems.

Zootaxa 3664 (3): 301–311 (27 May 2013)
Two new species of Cardiodectes Wilson, 1917 (Copepoda: Siphonostomatoida: Pennellidae) from gobiid fishes (Actinopterygii: Perciformes) in the western Pacific Ocean
DAISUKE UYENO

Two new species of the genus Cardiodectes Wilson, 1917 (Siphonostomatoida: Pennellidae) are described based on females from gobiid fishes (Actinopterygii: Perciformes) in coastal waters of the Pacific Ocean. Both new species belong to the ‘rubosus’ group sharing a trunk without an abdomen. Cardiodectes bellwoodi n. sp. parasitizes Istigobius nigroocellatus (Günther) in Australian waters and differs from members of the ‘rubosus’ group by having a trunk length less than twice its width, and a pair of large anterior lobes with branched processes. Cardiodectes shini n. sp. is similar to C. asper Uyeno & Nagasawa but is distinguishable by the presence of a well-developed, bilobed process between the bases
of the maxillae, and by the cephalothorax bearing only two pairs of lobes.

Zootaxa 3664 (3): 312–320 (27 May 2013)
Review of the systematic status of Sceloporus arenicolus Degenhardt and Jones, 1972 with an estimate of divergence time
LAUREN M. CHAN, JAMES W. ARCHIE, ANNE D. YODER & LEE A. FITZGERALD

The sagebrush lizards (Sceloporus graciosus group) consist of four taxa (S. graciosus graciosus, S. graciosus gracilis, S. graciosus vandenburgianus, and S. arenicolus) distributed in western North America. Of these, S. arenicolus is morphologically, behaviorally, and ecologically distinct as well as geographically disjunct from the other taxa, occurring only in the Mescalero-Monahans Sandhills of southeastern New Mexico and adjacent Texas. Sceloporus arenicolus is a taxon of concern because of its small range and habitat alteration due to land use practices. Understanding evolutionary relationships
among members of the S. graciosus group, and especially S. arenicolus, has important implications for conservation.
We examine the phylogenetic relationship of S. arenicolus relative to the three recognized subspecies of S. graciosus at mitochondrial and nuclear loci for populations sampled throughout the ranges of these taxa. Additionally, we estimate the divergence time and clade age of S. arenicolus. We find that the S. graciosus group is in need of major taxonomic revision, and also confirm that S. arenicolus is a genetically distinct and divergent lineage. These results bear important consequences for conservation and management.

Zootaxa 3664 (3): 361–368 (27 May 2013)
A new miniature species of Characidium Reinhardt (Ostariophysi: Characiformes: Crenuchidae) from the headwaters of the rio Araguaia, Brazil
ANDRÉ L. NETTO-FERREIRA, JOSÉ L. O. BIRINDELLI & PAULO A. BUCKUP

Characidium mirim is described from the rio das Mortes, rio Araguaia basin in Central Brazil. The new species is distinguished from its congeners by having an incomplete lateral line, a conspicuous dark longitudinal stripe and dark transverse bars not extending ventrally to the lateral line, and by lacking the adipose fin and the dark caudal blotch. A phylogenetic hypothesis based on the available data on the phylogenetic relationships of the subfamily Characidiinae is presented. Results suggest that the new species is closely related to C. bahiensis, C. interruptum, C. lagosantense, C. nupelia, C. lanei,
C. laterale, C. occidentale, C. orientale, C. rachovii, C. stigmosum, C. vestigipinne and C. xavante.

Zootaxa 3664 (3): 369–376 (27 May 2013)
New species of Pyrrhulina (Ostariophysi: Characiformes: Lebiasinidae) from the Brazilian Shield, with comments on a putative monophyletic group of species in the genus
ANDRÉ L. NETTO-FERREIRA & MANOELA M. F. MARINHO

Pyrrhulina marilynae, new species, is described. The new species can be distinguished among congeners mainly by presenting a conspicuous, dark, zigzag shaped primary stripe, extending to distal end of median caudal-fin rays, reduction of the number of precaudal vertebrae, absence of postcleithrum 2, and nine principal rays on caudal-fin dorsal lobe. The putative relationship of the new species with Pyrrhulina australis, P. vittata and P. zigzag, three small-sized species of the genus, is discussed.

Zootaxa 3664 (4): 505–524 (28 May 2013)
Cryptic speciation within Asthenodipsas vertebralis (Boulenger, 1900) (Squamata: Pareatidae), the description of a new species from Peninsular Malaysia, and the resurrection of A. tropidonotus (Lidth de Jude, 1923) from Sumatra: an integrative taxonomic analysis
ARIEL I. LOREDO, PERRY L. WOOD, JR., EVAN S. H. QUAH, SHAHRUL ANUAR, LEE F. GREER, NORHAYATI AHMAD & L. LEE GRISMER

A review of the taxonomic status of the Asian Slug Snake, Asthenodipsas vertebralis (Boulenger, 1900) based on an integrative taxonomic approach using molecular, morphological, color pattern, and ecological data indicate it is composed of three well supported monophyletic lineages: (1) Pulau Tioman and Fraser’s Hill, Pahang and Bukit Larut, Perak; Peninsular Malaysia; (2) its sister lineage from Northern Sumatra; and (3) the remaining basal lineage from Peninsular Malaysia.
Furthermore, we consider the high sequence divergence (6.3%–10.2%) between these lineages (especially in areas of sympatry) and discrete differences in their morphology, color pattern, and microhabitat preference as evidence they are not conspecific. As such, we resurrect the name A. tropidonotus (Lidth de Jeude, 1923) for the Sumatra populations, restrict the name A. vertebralis to the populations from Pulau Tioman, Genting Highlands, Fraser’s Hill, Gunung Benom, and Bukit Larut that contain terrestrial, banded adults; and consider A. lasgalenensis sp. nov. to be restricted to the populations
from Fraser’s Hill, Cameron Highlands, and Bukit Larut that contain arboreal, unbanded adults.

Zootaxa 3664 (4): 537–553 (28 May 2013)
Two new subspecies of the leaf-tailed gecko Phyllurus ossa (Lacertilia: Carphodactylidae) from mid-eastern Queensland, Australia
PATRICK COUPER & CONRAD J. HOSKIN

Following the discovery of a new population of Phyllurus ossa on Whitsunday Island in the Cumberland Island Group, eastern Queensland, we conducted both genetic and morphological analyses to assess differences between all known populations.
The analyses revealed three genetically distinct, morphologically diagnosable, geographical units. The differences are such that we recognise these as subspecies: Phyllurus ossa ossa restricted to the Mt Ossa/Mt Pelion/ Mt Charlton/St Helens Gap area; P. ossa hobsoni subsp. nov. on Mt Dryander and in the Conway Range and P. ossa tamoya subsp. nov. currently only known from Whitsunday Island. There are now 11 recognised taxa in Phyllurus. The three P. ossa subspecies are narrowly distributed and closely associated with exposed rock in low to mid-elevation vine forests. Their current distributions are shaped by past climate change that progressively contracted and fragmented the distribution of
rainforests in eastern Australia. The recognition of these subspecies has land management/conservation implications.

Scheffers, B. R., Brunner, R. M., Ramirez, S. D., Shoo, L. P., Diesmos, A. and Williams, S. E. (2013), Thermal Buffering of Microhabitats is a Critical Factor Mediating Warming Vulnerability of Frogs in the Philippine Biodiversity Hotspot. Biotropica. doi: 10.1111/btp.12042
Species may circumvent the impacts of climate warming if the habitats they use reduce ambient temperature. In this study, we identified which frog species from a tropical montane rain forest in the Philippines may be vulnerable to climate warming. To do so, we selected five anuran species that utilize four breeding habitats and identified the sensitivity and exposure of tadpoles and direct-developer eggs to heat by measuring their critical thermal maximums (CTmax) and the habitat-specific temperatures they experience. Our study species included two direct-developer frogs—one species that lays its eggs on exposed leaves, and another that lays its eggs in ferns—and three species that produce aquatic free-swimming tadpoles—two stream breeders, and one phytotelm (tree hole) breeder. We compared thermal tolerances derived from microclimates of breeding habitats with tolerances derived from macroclimate (i.e., non-buffered air temperature taken from the rain forest canopy). We also examined whether differences in CTmax existed across life-history stages (egg, metamorph/young-of-year, and adult) for the two direct-developer frog species. Habitats buffered ambient temperature and expanded thermal tolerances of all frog species. We found that direct-developers, however, are more vulnerable to increased temperatures than aquatic breeders—indicated by their high sensitivity to temperature, and exposure to high temperatures. Direct-developer eggs were more sensitive to warming than both metamorph and adult life-history stages. Thermally buffered microhabitats may represent the only protection against current and impending climate warming. Our data highlight the importance of considering sensitivity and exposure in unison when deciphering warming vulnerability of frogs. We therefore examined whether warming vulnerability varied by life-history stage for select species.

David Benhaïm, René Guyomard, Béatrice Chatain, Edwige Quillet, Marie-Laure Bégout, Genetic differences for behaviour in juveniles from two strains of brown trout suggest an effect of domestication history, Applied Animal Behaviour Science, Available online 27 May 2013, ISSN 0168-1591, 10.1016/j.applanim.2013.04.022.
Because captivity constitutes a drastic environmental change, domestication is expected to induce a rapid genetic selection for behavioural traits. In this study, we searched for genetic differences in behaviour among brown trout juveniles from two strains differing for their domestication history, i.e. an almost pure native wild Mediterranean population (W) and an Atlantic domesticated strain (D). In order to assess pure genetic differences among strains, males from the two origins were mated with Mediterranean females to produce two experimental crosses (WW and WD). The swimming activity characteristics of individual WW and WD juveniles were compared before and after the application of a stress (light switched off suddenly, followed by a 5-min period of darkness). For each of the fish observed, mating type origin (WW or WD) was unambiguously reassigned by genotyping. Behavioural responses differed between WD and WW fish. Angular velocity and the time spent immobile were greater for WW fish both before and after the short period of darkness, indicating higher reactivity. Once the light had been turned on again, mean velocity and total distance travelled were higher in WD than in WW fish. WD fish tended to recover levels of swimming activity higher than those before the dark period. This study therefore demonstrates an impact of genetic origin and domestication on swimming activity repertoire (higher reactivity in WW fish), a behavioural trait of particular importance for individual ecological performance. Owing to the contrasted domestication history of the two strains used in the comparison, we assume that the domestication level largely contributes to the behavioural changes observed.

David C. Collar, Crystal M. Reynaga, Andrea B. Ward, Rita S. Mehta, A revised metric for quantifying body shape in vertebrates, Zoology, Available online 27 May 2013, ISSN 0944-2006, 10.1016/j.zool.2013.03.001.
Vertebrates exhibit tremendous diversity in body shape, though quantifying this variation has been challenging. In the past, researchers have used simplified metrics that either describe overall shape but reveal little about its anatomical basis or that characterize only a subset of the morphological features that contribute to shape variation. Here, we present a revised metric of body shape, the vertebrate shape index (VSI), which combines the four primary morphological components that lead to shape diversity in vertebrates: head shape, length of the second major body axis (depth or width), and shape of the precaudal and caudal regions of the vertebral column. We illustrate the usefulness of VSI on a data set of 194 species, primarily representing five major vertebrate clades: Actinopterygii, Lissamphibia, Squamata, Aves, and Mammalia. We quantify VSI diversity within each of these clades and, in the course of doing so, show how measurements of the morphological components of VSI can be obtained from radiographs, articulated skeletons, and cleared and stained specimens. We also demonstrate that head shape, secondary body axis, and vertebral characteristics are important independent contributors to body shape diversity, though their importance varies across vertebrate groups. Finally, we present a functional application of VSI to test a hypothesized relationship between body shape and the degree of axial bending associated with locomotor modes in ray-finned fishes. Altogether, our study highlights the promise VSI holds for identifying the morphological variation underlying body shape diversity as well as the selective factors driving shape evolution.

Juan J. Luque-Larena, Francois Mougeot, Javier Viñuela, Daniel Jareño, Leticia Arroyo, Xavier Lambin, Beatriz Arroyo, Recent large-scale range expansion and outbreaks of the common vole (Microtus arvalis) in NW Spain, Basic and Applied Ecology, Available online 27 May 2013, ISSN 1439-1791, 10.1016/j.baae.2013.04.006.
Irruptive populations of rodents cause damage to agriculture worldwide. By the end of the last century, the distribution range of Microtus arvalis in NW Spain greatly expanded to encompass agricultural habitats, with the appearance of crop damaging population outbreaks. The absence of long term vole monitoring data has so far precluded outbreak forecasting, which might help mitigating associated bioeconomic costs. We used non-standard and diverse sources of information, including newspaper and national technical reports, to describe the vole expansion and outbreak dynamics in NW Spain since the late 1960s. We illustrate a rapid and large scale colonisation of agricultural lowlands, and suggest a pattern of westward expansion emanating from the peripheral mountains. Crop damaging outbreaks directly followed range expansion and our analyses indicate that they have occurred at approximately 5-year intervals since the early 1980s. This is the first description of long term (>40 years) regional scale vole dynamics reported for the Iberian Peninsula. We suggest that expansion from (humid) mountains to (dry) plains may be related to recent changes in land use. If confirmed at a local scale, the apparent cyclicity of outbreaks would provide a basis for forecasting outbreak risk in NW Spain and may help managers adjust current control strategies.

Maria Luisa S.P. Jorge, Mauro Galetti, Milton C. Ribeiro, Katia Maria P.M.B. Ferraz, Mammal defaunation as surrogate of trophic cascades in a biodiversity hotspot, Biological Conservation, Available online 27 May 2013, ISSN 0006-3207, 10.1016/j.biocon.2013.04.018.
Preserving large tracts of natural habitats is essential to maintain biodiversity. Nevertheless, even large areas may still suffer from less “visible” impacts such as loss of ecological processes. Because mapping ecological processes over large scales is not practical, an alternative is to map surrogate species that are key for those processes. In this study, we chose four species of Neotropical large mammals (the largest apex predator: jaguar – Panthera onca; the largest herbivore: tapir – Tapirus terrestris; the largest seed predator: white-lipped peccary – Tayassu pecari; and the largest arboreal seed disperser: muriqui – Brachyteles spp.) in an ecosystem with an old history of human impact (the Atlantic Forest) to test whether areas with native forest still harbor ecological processes that may guarantee long-term ecosystem maintenance. We gathered 94 locations with recent presence of the four species to map current ranges and model suitable areas. Our results reveal that 96% of the remaining Atlantic Forest is depleted of at least one of the four surrogate species and 88% is completely depleted of all four surrogate species. We also found that only 16% is still environmentally suitable for all four, and 55% is completely unsuitable to all four of them. Our study highlights the importance of looking beyond land cover to fully depict intactness of natural areas, and suggests that ecosystems with a long history of human impact (such as the Atlantic Forest) may be suffering from ecological impacts not seen at a first glance.

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