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1.  Continental variation in relative hippocampal volume in birds: the phylogenetic extent of the effect and the potential role of winter temperatures 
Biology letters  2005;1(3):330-333.
Hippocampal (HC) volume has been hypothesized to increase with an increase in food-hoarding specialization in corvids and parids. Recent studies revealed that (i) the HC/hoarding relationship is significant when a difference in HC volume between Eurasian and North American species is controlled for and (ii) the evolutionary association has been acting on a broader phylogenetic context involving avian families outside the Corvidae and Paridae. However, the phylogenetic extent of the continent effect has not been previously addressed. Using data representing 48 avian species, we performed a phylogenetic analysis to test if continental effects are important in a wider evolutionary spectrum. Our results support the observation that Eurasian species have generally larger HC than North American species if variation in food hoarding, which also varied between continents, was held constant. Surprisingly, the relationship between continental distribution and relative HC volume was significant when we included only non-hoarding families in our analysis, indicating that the extent of the continent effect is much broader than originally described. We investigated the potential role of minimal winter temperatures at the northernmost distribution borders in mediating continent effects. The effect of winter temperatures on HC volume was weak and it did not vary consistently along continents. We suggest that the general continental differences in relative HC size are independent of food hoarding and that its determinants should be sought among other ecological factors and life-history traits.
doi:10.1098/rsbl.2005.0328
PMCID: PMC1523380  PMID: 16878181
Corvidae; food caching; hippocampus; Paridae; phylogeny
2.  Does hippocampal size correlate with the degree of caching specialization? 
A correlation between the degree of specialization for food hoarding and the volume of the hippocampal formation in passerine birds has been accepted for over a decade. The relationship was first demonstrated in family-level comparisons, and subsequently in species comparisons within two families containing a large number of hoarding species, the Corvidae and the Paridae. Recently, this approach has been criticized as invalid and excessively adaptationist. A recent test of the predicted trends with data pooled from previous studies found no evidence for such a correlation in either of these two families. This result has been interpreted as support for the critique. Here we reanalyse the original dataset and also include additional new data on several parid species. Our results show a surprising difference between continents, with North American species possessing significantly smaller hippocampi than Eurasian ones. Controlling for the continent effect makes the hoarding capacity/hippocampal formation correlation clearly significant in both families. We discuss possible reasons for the continent effect.
doi:10.1098/rspb.2004.2912
PMCID: PMC1523289  PMID: 15590591
hippocampus; hippocampal formation; neuroecology; Paridae; Corvidae
3.  Does hippocampal size correlate with the degree of caching specialization? 
A correlation between the degree of specialization for food hoarding and the volume of the hippocampal formation in passerine birds has been accepted for over a decade. The relationship was first demonstrated in family-level comparisons, and subsequently in species comparisons within two families containing a large number of hoarding species, the Corvidae and the Paridae. Recently, this approach has been criticized as invalid and excessively adaptationist. A recent test of the predicted trends with data pooled from previous studies found no evidence for such a correlation in either of these two families. This result has been interpreted as support for the critique. Here we reanalyse the original dataset and also include additional new data on several parid species. Our results show a surprising difference between continents, with North American species possessing significantly smaller hippocampi than Eurasian ones. Controlling for the continent effect makes the hoarding capacity/hippocampal formation correlation clearly significant in both families. We discuss possible reasons for the continent effect.
doi:10.1098/rspb.2004.2912
PMCID: PMC1523289  PMID: 15590591
4.  Is hippocampal volume affected by specialization for food hoarding in birds? 
The hypothesis that spatial-memory specialization affects the size of the hippocampus has become widely accepted among scientists. The hypothesis comes from studies on birds primarily in two families, the Paridae (tits, titmice and chickadees) and the Corvidae (crows, nutcrackers, jays, etc.). Many species in these families store food and rely on spatial memory to relocate the cached items. The hippocampus is a brain structure that is thought to be important for memory. Several studies report that hoarding species in these families possess larger hippocampi than non-hoarding relatives, and that species classified as large-scale hoarders have larger hippocampi than less specialized hoarders. We have investigated the largest dataset on hippocampus size and food-hoarding behaviour in these families so far but did not find a significant correlation between food-hoarding specialization and hippocampal volume. The occurrence of such an effect in earlier studies may depend on differences in the estimation of hippocampal volumes or difficulties in categorizing the degree of specialization for hoarding or both. To control for discrepancies in measurement methods we made our own estimates of hippocampal volumes in 16 individuals of four species that have been included in previous studies. Our estimates agreed closely with previous ones, suggesting that measurement methods are sufficiently consistent. Instead, the main reasons that previous studies have found an effect where we did not are difficulties in assessing the degree of hoarding specialization and the fact that smaller subsets of species were compared than in our study. Our results show that a correlation between food-hoarding specialization and hippocampal volume cannot be claimed on the basis of present data in these families.
doi:10.1098/rspb.2003.2413
PMCID: PMC1691419  PMID: 12908975
5.  An evolutionary perspective on caching by corvids 
A principal finding in the food-caching literature is that species differences in hoarding propensity are positively correlated with species differences in degree of adaptations to caching behaviour, such as performance on spatial memory tasks and hippocampal volume. However, there are examples that do not fit this pattern. We argue that these examples can be better understood by considering the phylogenetic relatedness between species. We reconstruct the ancestral state for caching behaviour in corvids and assess when transitions in caching behaviour occurred within the corvid phylogeny. Our analysis shows that the common ancestor of all corvids was a moderate cacher. This result suggests that corvids followed a bi-directional evolutionary trajectory in which caching was secondarily lost twice and there were at least two independent transitions from moderate to specialized caching. The independent evolution of specialized cachers in the two groups must, therefore, be a case of convergent evolution. This is exemplified by the fact that specialized cachers show structurally different adaptations serving the same function to intense caching, such as different pouches to transport food. Finally, we argue that convergent evolution may have led to adaptations in memory and hippocampus that serve the same function but differ in design, and that these different adaptations may explain the examples that do not fit the pattern predicted by the adaptive specialization hypothesis.
doi:10.1098/rspb.2005.3350
PMCID: PMC1560201  PMID: 16615207
spatial memory; hippocampus; adaptive specialization; food hoarding; phylogeny; corvid
6.  Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus 
A well-developed spatial memory is important for many animals, but appears especially important for scatter-hoarding species. Consequently, the scatter-hoarding system provides an excellent paradigm in which to study the integrative aspects of memory use within an ecological and evolutionary framework. One of the main tenets of this paradigm is that selection for enhanced spatial memory for cache locations should specialize the brain areas involved in memory. One such brain area is the hippocampus (Hp). Many studies have examined this adaptive specialization hypothesis, typically relating spatial memory to Hp volume. However, it is unclear how the volume of the Hp is related to its function for spatial memory. Thus, the goal of this article is to evaluate volume as a main measurement of the degree of morphological and physiological adaptation of the Hp as it relates to memory. We will briefly review the evidence for the specialization of memory in food-hoarding animals and discuss the philosophy behind volume as the main currency. We will then examine the problems associated with this approach, attempting to understand the advantages and limitations of using volume and discuss alternatives that might yield more specific hypotheses. Overall, there is strong evidence that the Hp is involved in the specialization of spatial memory in scatter-hoarding animals. However, volume may be only a coarse proxy for more relevant and subtle changes in the structure of the brain underlying changes in behaviour. To better understand the nature of this brain/memory relationship, we suggest focusing on more specific and relevant features of the Hp, such as the number or size of neurons, variation in connectivity depending on dendritic and axonal arborization and the number of synapses. These should generate more specific hypotheses derived from a solid theoretical background and should provide a better understanding of both neural mechanisms of memory and their evolution.
doi:10.1098/rstb.2009.0208
PMCID: PMC2830242  PMID: 20156816
birds; comparative analysis; food caching; neuroecology; stereology
7.  Cholecystokinin-33 acutely attenuates food foraging, hoarding and intake in Siberian hamsters 
Peptides  2009;31(4):618-624.
Neurochemicals that stimulate food foraging and hoarding in Siberian hamsters are becoming more apparent, but we do not know if cessation of these behaviors is due to waning of excitatory stimuli and/or the advent of inhibitory factors. Cholecystokinin (CCK) may be such an inhibitory factor as it is the prototypic gastrointestinal satiety peptide and is physiologically important in decreasing food intake in several species including Siberian hamsters. Systemic injection of CCK-33 in laboratory rats decreases food intake, doing so to a greater extent than CCK-8. We found minimal effects of CCK-8 on food foraging and hoarding previously in Siberian hamsters, but have not tested CCK-33. Therefore, we asked: Does CCK-33 decrease normal levels or food deprivation-induced increases in food foraging, hoarding and intake? Hamsters were housed in a wheel running-based foraging system with simulated burrows to test the effects of peripheral injections of CCK-33 (13.2, 26.4, or 52.8 μg/kg body mass), with or without a preceding 56 h food deprivation. The highest dose of CCK-33 caused large baseline reductions in all three behaviors for the 1st h post injection compared with saline; in addition, the intermediate CCK-33 dose was sufficient to curtail food intake and foraging during the 1st h. In food deprived hamsters, we used a 52.8 μg/kg body mass dose of CCK-33 which decreased food intake, hoarding, and foraging almost completely compared with saline controls for 1 h. Therefore, CCK-33 appears to be a potent inhibitor of food intake, hoarding, and foraging in Siberian hamsters.
doi:10.1016/j.peptides.2009.12.010
PMCID: PMC2837760  PMID: 20025915
appetitive behavior; consummatory behavior; injection; satiety
8.  Food Availability and Animal Space Use Both Determine Cache Density of Eurasian Red Squirrels 
PLoS ONE  2013;8(11):e80632.
Scatter hoarders are not able to defend their caches. A longer hoarding distance combined with lower cache density can reduce cache losses but increase the costs of hoarding and retrieving. Scatter hoarders arrange their cache density to achieve an optimal balance between hoarding costs and main cache losses. We conducted systematic cache sampling investigations to estimate the effects of food availability on cache patterns of Eurasian red squirrels (Sciurus vulgaris). This study was conducted over a five-year period at two sample plots in a Korean pine (Pinus koraiensis)-dominated forest with contrasting seed production patterns. During these investigations, the locations of nest trees were treated as indicators of squirrel space use to explore how space use affected cache pattern. The squirrels selectively hoarded heavier pine seeds farther away from seed-bearing trees. The heaviest seeds were placed in caches around nest trees regardless of the nest tree location, and this placement was not in response to decreased food availability. The cache density declined with the hoarding distance. Cache density was lower at sites with lower seed production and during poor seed years. During seed mast years, the cache density around nest trees was higher and invariant. The pine seeds were dispersed over a larger distance when seed availability was lower. Our results suggest that 1) animal space use is an important factor that affects food hoarding distance and associated cache densities, 2) animals employ different hoarding strategies based on food availability, and 3) seed dispersal outside the original stand is stimulated in poor seed years.
doi:10.1371/journal.pone.0080632
PMCID: PMC3827212  PMID: 24265833
9.  Avian influenza at both ends of a migratory flyway: characterizing viral genomic diversity to optimize surveillance plans for North America 
Evolutionary Applications  2009;2(4):457-468.
Although continental populations of avian influenza viruses are genetically distinct, transcontinental reassortment in low pathogenic avian influenza (LPAI) viruses has been detected in migratory birds. Thus, genomic analyses of LPAI viruses could serve as an approach to prioritize species and regions targeted by North American surveillance activities for foreign origin highly pathogenic avian influenza (HPAI). To assess the applicability of this approach, we conducted a phylogenetic and population genetic analysis of 68 viral genomes isolated from the northern pintail (Anas acuta) at opposite ends of the Pacific migratory flyway in North America. We found limited evidence for Asian LPAI lineages on wintering areas used by northern pintails in California in contrast to a higher frequency on breeding locales of Alaska. Our results indicate that the number of Asian LPAI lineages observed in Alaskan northern pintails, and the nucleotide composition of LPAI lineages, is not maintained through fall migration. Accordingly, our data indicate that surveillance of Pacific Flyway northern pintails to detect foreign avian influenza viruses would be most effective in Alaska. North American surveillance plans could be optimized through an analysis of LPAI genomics from species that demonstrate evolutionary linkages with European or Asian lineages and in regions that have overlapping migratory flyways with areas of HPAI outbreaks.
doi:10.1111/j.1752-4571.2009.00071.x
PMCID: PMC3352445
avian influenza; genetic; low pathogenic; migration; northern pintail; virus; waterfowl
10.  Are subspecies useful in evolutionary and conservation biology? 
The taxonomic rank of subspecies remains highly contentious, largely because traditional subspecies boundaries have sometimes been contradicted by molecular phylogenetic data. The most complete meta-analysis to date, for instance, found that only 3% of traditional avian subspecies represented distinct phylogenetic lineages. However, the global generality of this phenomenon remains unclear due to this previous study's narrow geographic focus on continental Nearctic and Palearctic subspecies. Here, we present a new global analysis of avian subspecies and show that 36% of avian subspecies are, in fact, phylogenetically distinct. Among biogeographic realms we find significant differences in the proportion of subspecies that are phylogenetically distinct, with Nearctic/Palearctic subspecies showing significantly reduced levels of differentiation. Additionally, there are differences between island and continental subspecies, with continental subspecies significantly less likely to be genetically distinct. These results indicate that the overall level of congruence between taxonomic subspecies and molecular phylogenetic data is greater than previously thought. We suggest that the widespread impression that avian subspecies are not real arises from a predominance of studies focusing on continental subspecies in North America and Eurasia, regions which show unusually low levels of genetic differentiation. The broader picture is that avian subspecies often provide an effective short-cut for estimating patterns of intraspecific genetic diversity, thereby providing a useful tool for the study of evolutionary divergence and conservation.
doi:10.1098/rspb.2005.3425
PMCID: PMC1560251  PMID: 16600880
subspecies; birds; phylogenetics; monophyly; islands
11.  Integrating ecology, psychology and neurobiology within a food-hoarding paradigm 
Many animals regularly hoard food for future use, which appears to be an important adaptation to a seasonally and/or unpredictably changing environment. This food-hoarding paradigm is an excellent example of a natural system that has broadly influenced both theoretical and empirical work in the field of biology. The food-hoarding paradigm has played a major role in the conceptual framework of numerous fields from ecology (e.g. plant–animal interactions) and evolution (e.g. the coevolution of caching, spatial memory and the hippocampus) to psychology (e.g. memory and cognition) and neurobiology (e.g. neurogenesis and the neurobiology of learning and memory). Many food-hoarding animals retrieve caches by using spatial memory. This memory-based behavioural system has the inherent advantage of being tractable for study in both the field and laboratory and has been shaped by natural selection, which produces variation with strong fitness consequences in a variety of taxa. Thus, food hoarding is an excellent model for a highly integrative approach to understanding numerous questions across a variety of disciplines. Recently, there has been a surge of interest in the complexity of animal cognition such as future planning and episodic-like-memory as well as in the relationship between memory, the environment and the brain. In addition, new breakthroughs in neurobiology have enhanced our ability to address the mechanisms underlying these behaviours. Consequently, the field is necessarily becoming more integrative by assessing behavioural questions in the context of natural ecological systems and by addressing mechanisms through neurobiology and psychology, but, importantly, within an evolutionary and ecological framework. In this issue, we aim to bring together a series of papers providing a modern synthesis of ecology, psychology, physiology and neurobiology and identifying new directions and developments in the use of food-hoarding animals as a model system.
doi:10.1098/rstb.2009.0216
PMCID: PMC2830247  PMID: 20156812
food hoarding; memory; seed dispersal; neurogenesis; hippocampus; cognition
12.  Biotic Interactions Overrule Plant Responses to Climate, Depending on the Species' Biogeography 
PLoS ONE  2014;9(10):e111023.
This study presents an experimental approach to assess the relative importance of climatic and biotic factors as determinants of species' geographical distributions. We asked to what extent responses of grassland plant species to biotic interactions vary with climate, and to what degree this variation depends on the species' biogeography. Using a gradient from oceanic to continental climate represented by nine common garden transplant sites in Germany, we experimentally tested whether congeneric grassland species of different geographic distribution (oceanic vs. continental plant range type) responded differently to combinations of climate, competition and mollusc herbivory. We found the relative importance of biotic interactions and climate to vary between the different components of plant performance. While survival and plant height increased with precipitation, temperature had no effect on plant performance. Additionally, species with continental plant range type increased their growth in more benign climatic conditions, while those with oceanic range type were largely unable to take a similar advantage of better climatic conditions. Competition generally caused strong reductions of aboveground biomass and growth. In contrast, herbivory had minor effects on survival and growth. Against expectation, these negative effects of competition and herbivory were not mitigated under more stressful continental climate conditions. In conclusion we suggest variation in relative importance of climate and biotic interactions on broader scales, mediated via species-specific sensitivities and factor-specific response patterns. Our results have important implications for species distribution models, as they emphasize the large-scale impact of biotic interactions on plant distribution patterns and the necessity to take plant range types into account.
doi:10.1371/journal.pone.0111023
PMCID: PMC4214694  PMID: 25356912
13.  The history of scatter hoarding studies 
In this review, I will present an overview of the development of the field of scatter hoarding studies. Scatter hoarding is a conspicuous behaviour and it has been observed by humans for a long time. Apart from an exceptional experimental study already published in 1720, it started with observational field studies of scatter hoarding birds in the 1940s. Driven by a general interest in birds, several ornithologists made large-scale studies of hoarding behaviour in species such as nutcrackers and boreal titmice. Scatter hoarding birds seem to remember caching locations accurately, and it was shown in the 1960s that successful retrieval is dependent on a specific part of the brain, the hippocampus. The study of scatter hoarding, spatial memory and the hippocampus has since then developed into a study system for evolutionary studies of spatial memory. In 1978, a game theoretical paper started the era of modern studies by establishing that a recovery advantage is necessary for individual hoarders for the evolution of a hoarding strategy. The same year, a combined theoretical and empirical study on scatter hoarding squirrels investigated how caches should be spaced out in order to minimize cache loss, a phenomenon sometimes called optimal cache density theory. Since then, the scatter hoarding paradigm has branched into a number of different fields: (i) theoretical and empirical studies of the evolution of hoarding, (ii) field studies with modern sampling methods, (iii) studies of the precise nature of the caching memory, (iv) a variety of studies of caching memory and its relationship to the hippocampus. Scatter hoarding has also been the subject of studies of (v) coevolution between scatter hoarding animals and the plants that are dispersed by these.
doi:10.1098/rstb.2009.0217
PMCID: PMC2830248  PMID: 20156813
scatter hoarding; cache retrieval; spatial memory; optimal cache density; hippocampus
14.  Prevalence, Comorbidity and Heritability of Hoarding Symptoms in Adolescence: A Population Based Twin Study in 15-Year Olds 
PLoS ONE  2013;8(7):e69140.
Background
Hoarding Disorder (HD) is often assumed to be an ‘old age’ problem, but many individuals diagnosed with HD retrospectively report first experiencing symptoms in childhood or adolescence. We examined the prevalence, comorbidity and etiology of hoarding symptoms in adolescence.
Methods
To determine the presence of clinically significant hoarding symptoms, a population-based sample of 15-year old twins (N = 3,974) completed the Hoarding Rating Scale-Self Report. Co-occurring Obsessive Compulsive Disorder (OCD), Autism Spectrum Disorders (ASD) and Attention Deficit Hyperactivity Disorder (ADHD) were estimated from parental report. Model-fitting analyses divided hoarding symptom scores into additive genetic, shared, and non-shared environmental effects.
Results
The prevalence of clinically significant hoarding symptoms was 2% (95% CI 1.6–2.5%), with a significantly higher prevalence in girls than boys. Exclusion of the clutter criterion (as adolescents do not have control over their environment) increased the prevalence rate to 3.7% (95% CI 3.1–4.3%). Excessive acquisition was reported by 30–40% among those with clinically significant hoarding symptoms. The prevalence of co-occurring OCD (2.9%), ASD (2.9%) and ADHD (10.0%) was comparable in hoarding and non-hoarding teenagers. Model-fitting analyses suggested that, in boys, additive genetic (32%; 95% CI 13–44%) and non-shared environmental effects accounted for most of the variance. In contrast, among girls, shared and non-shared environmental effects explained most of the variance, while additive genetic factors played a negligible role.
Conclusions
Hoarding symptoms are relatively prevalent in adolescents, particularly in girls, and cause distress and/or impairment. Hoarding was rarely associated with other common neurodevelopmental disorders, supporting its DSM-5 status as an independent diagnosis. The relative importance of genetic and shared environmental factors for hoarding differed across sexes. The findings are suggestive of dynamic developmental genetic and environmental effects operating from adolescence onto adulthood.
doi:10.1371/journal.pone.0069140
PMCID: PMC3707873  PMID: 23874893
15.  PYY(3–36) Into The Arcuate Nucleus Inhibits Food Deprivation-Induced Increases In Food Hoarding and Intake 
Peptides  2013;0:20-28.
Central administration of neuropeptide Y (NPY) increases food intake in laboratory rats and mice, as well as food foraging and hoarding in Siberian hamsters. The NPY-Y1 and Y5 receptors (Rs) within the hypothalamus appear sufficient to account for these increases in ingestive behaviors. Stimulation of NPY-Y2Rs in the Arcuate nucleus (Arc) has an anorexigenic effect as shown by central or peripheral administration of its natural ligand peptide YY (3–36) and pharmacological NPY-Y2R antagonism by BIIE0246 increases food intake. Both effects on food intake by NPY-Y2R agonism and antagonism are relatively short-lived lasting ~4 h. The role of NPY-Y2Rs in appetitive ingestive behaviors (food foraging/hoarding) is untested, however. Therefore, Siberians hamsters, a natural food hoarder, were housed in a semi-natural burrow/foraging system that had a) foraging requirement (10 revolutions/ pellet), no free food (true foraging group), b) no running wheel access, free food (general malaise control) or c) running wheel access, free food (exercise control). We microinjected BIIE0246 (antagonist) and PYY(3–36) (agonist) into the Arc to test the role of NPY-Y2Rs there on ingestive behaviors. Food foraging, hoarding, and intake were not affected by Arc BIIE0246 microinjection in fed hamsters 1, 2, 4, and 24 h post injection. Stimulation of NPY-Y2Rs by PYY(3–36) inhibited food intake at 0–1 and 1–2 h and food hoarding at 1–2 h without causing general malaise or affecting foraging. Collectively, these results implicate a sufficiency, but not necessity, of the Arc NPY-Y2R in the inhibition of food intake and food hoarding by Siberian hamsters.
doi:10.1016/j.peptides.2013.05.005
PMCID: PMC3759582  PMID: 23816798
appetitive behavior; Siberian hamster; Peptide YY; BIIE0246; food foraging; food deprivation
16.  Vertebral Formula in Red-Crowned Crane (Grus japonensis) and Hooded Crane (Grus monacha) 
ABSTRACT
Red-crowned cranes (Grus japonensis) are distributed separately in the east Eurasian Continent (continental population) and in Hokkaido, Japan (island population). The island population is sedentary in eastern Hokkaido and has increased from a very small number of cranes to over 1,300, thus giving rise to the problem of poor genetic diversity. While, Hooded cranes (Grus monacha), which migrate from the east Eurasian Continent and winter mainly in Izumi, Kagoshima Prefecture, Japan, are about eight-time larger than the island population of Red-crowned cranes. We collected whole bodies of these two species, found dead or moribund in eastern Hokkaido and in Izumi, and observed skeletons with focus on vertebral formula. Numbers of cervical vertebrae (Cs), thoracic vertebrae (Ts), vertebrae composing the synsacrum (Sa) and free coccygeal vertebrae (free Cos) in 22 Red-crowned cranes were 17 or 18, 9–11, 13 or 14 and 7 or 8, respectively. Total number of vertebrae was 47, 48 or 49, and the vertebral formula was divided into three types including 9 sub-types. Numbers of Cs, Ts, vertebrae composing the Sa and free Cos in 25 Hooded cranes were 17 or 18, 9 or 10, 12–14 and 6–8, respectively. Total number of vertebrae was 46, 47, 48 or 49, and the vertebral formula was divided into four types including 14 sub-types. Our findings clearly showed various numerical vertebral patterns in both crane species; however, these variations in the vertebral formula may be unrelated to the genetic diversity.
doi:10.1292/jvms.13-0295
PMCID: PMC4064133  PMID: 24334828
cranes; vertebrae; wild animals
17.  Evolution, Systematics, and Phylogeography of Pleistocene Horses in the New World: A Molecular Perspective 
PLoS Biology  2005;3(8):e241.
The rich fossil record of horses has made them a classic example of evolutionary processes. However, while the overall picture of equid evolution is well known, the details are surprisingly poorly understood, especially for the later Pliocene and Pleistocene, c. 3 million to 0.01 million years (Ma) ago, and nowhere more so than in the Americas. There is no consensus on the number of equid species or even the number of lineages that existed in these continents. Likewise, the origin of the endemic South American genus Hippidion is unresolved, as is the phylogenetic position of the “stilt-legged” horses of North America. Using ancient DNA sequences, we show that, in contrast to current models based on morphology and a recent genetic study, Hippidion was phylogenetically close to the caballine (true) horses, with origins considerably more recent than the currently accepted date of c. 10 Ma. Furthermore, we show that stilt-legged horses, commonly regarded as Old World migrants related to the hemionid asses of Asia, were in fact an endemic North American lineage. Finally, our data suggest that there were fewer horse species in late Pleistocene North America than have been named on morphological grounds. Both caballine and stilt-legged lineages may each have comprised a single, wide-ranging species.
Ancient DNA simplifies the systematics of horses present in the New Word during the Pleistocene and reveals that the stilt- legged horse is native to the continent and not a Eurasian migrant.
doi:10.1371/journal.pbio.0030241
PMCID: PMC1159165  PMID: 15974804
18.  Continental phylogeography of an ecologically and morphologically diverse Neotropical songbird, Zonotrichia capensis 
Background
The Neotropics are exceptionally diverse, containing roughly one third of all extant bird species on Earth. This remarkable species richness is thought to be a consequence of processes associated with both Andean orogenesis throughout the Tertiary, and climatic fluctuations during the Quaternary. Phylogeographic studies allow insights into how such events might have influenced evolutionary trajectories of species and ultimately contribute to a better understanding of speciation. Studies on continentally distributed species are of particular interest because different populations of such taxa may show genetic signatures of events that impacted the continent-wide biota. Here we evaluate the genealogical history of one of the world’s most broadly-distributed and polytypic passerines, the rufous-collared sparrow (Zonotrichia capensis).
Results
We obtained control region DNA sequences from 92 Zonotrichia capensis individuals sampled across the species’ range (Central and South America). Six additional molecular markers, both nuclear and mitochondrial, were sequenced for a subset of individuals with divergent control region haplotypes. Median-joining network analysis, and Bayesian and maximum parsimony phylogenetic analyses all recovered three lineages: one spanning Middle America, the Dominican Republic, and north-western South America; one encompassing the Dominican Republic, Roraima (Venezuela) and La Paz (Bolivia) south to Tierra del Fuego, Argentina; and a third, including eastern Argentina and Brazil. Phylogenetic analyses suggest that the Middle American/north-western South American clade is sister to the remaining two. Bayesian and maximum likelihood coalescent simulations used to study lineage demographic history, diversification times, migration rates and population expansion together suggested that diversification of the three lineages occurred rapidly during the Pleistocene, with negligible gene flow, leaving genetic signatures of population expansions.
Conclusions
The Pleistocene history of the rufous-collared sparrow involved extensive range expansion from a probable Central American origin. Its remarkable morphological and behavioral diversity probably represents recent responses to local conditions overlying deeper patterns of lineage diversity, which are themselves produced by isolation and the history of colonization of South America.
doi:10.1186/1471-2148-13-58
PMCID: PMC3632491  PMID: 23452908
Colonization; Demographic expansion; Intraspecific divergence; DNA sequences; Pleistocene; Rufous-collared sparrow
19.  Phylogeography of the Microcoleus vaginatus (Cyanobacteria) from Three Continents – A Spatial and Temporal Characterization 
PLoS ONE  2012;7(6):e40153.
It has long been assumed that cyanobacteria have, as with other free-living microorganisms, a ubiquitous occurrence. Neither the geographical dispersal barriers nor allopatric speciation has been taken into account. We endeavoured to examine the spatial and temporal patterns of global distribution within populations of the cyanobacterium Microcoleus vaginatus, originated from three continents, and to evaluate the role of dispersal barriers in the evolution of free-living cyanobacteria. Complex phylogeographical approach was applied to assess the dispersal and evolutionary patterns in the cyanobacterium Microcoleus vaginatus (Oscillatoriales). We compared the 16S rRNA and 16S-23S ITS sequences of strains which had originated from three continents (North America, Europe, and Asia). The spatial distribution was investigated using a phylogenetic tree, network, as well as principal coordinate analysis (PCoA). A temporal characterization was inferred using molecular clocks, calibrated from fossil DNA. Data analysis revealed broad genetic diversity within M. vaginatus. Based on the phylogenetic tree, network, and PCoA analysis, the strains isolated in Europe were spatially separated from those which originated from Asia and North America. A chronogram showed a temporal limitation of dispersal barriers on the continental scale. Dispersal barriers and allopatric speciation had an important role in the evolution of M. vaginatus. However, these dispersal barriers did not have a permanent character; therefore, the genetic flow among populations on a continental scale was only temporarily present. Furthermore, M. vaginatus is a recently evolved species, which has been going through substantial evolutionary changes.
doi:10.1371/journal.pone.0040153
PMCID: PMC3384635  PMID: 22761955
20.  How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals 
Some plants that are dispersed by scatter-hoarding animals appear to have evolved the ability to manipulate the behaviour of those animals to increase the likelihood that seeds and nuts will be stored and that a portion of those items will not be recovered. Plants have achieved this in at least four ways. First, by producing large, nutritious seeds and nuts that are attractive to animals and that stimulate hoarding behaviour. Second, by imposing handling costs that cause animals to hoard rather than to eat items immediately. These handling costs can take one of two forms: physical barriers (e.g. hard seed coats) that take time to remove and secondary chemicals (e.g. tannins) that impose metabolic costs. Third, by masting, where a population of plants synchronizes reproductive effort, producing large nut crops at intervals of several years. Mast crops not only satiate seed predators, but also increase the amount of seed dispersal because scatter-hoarding animals are not easily satiated during caching (causing animals to store more food than they can consume) but are satiated during cache recovery. And fourth, by producing seeds that do not emit strong odours so that buried seeds are less likely to be discovered. These, and perhaps other, traits have increased the relative success of plant species with seeds dispersed by scatter-hoarding animals.
doi:10.1098/rstb.2009.0205
PMCID: PMC2830241  PMID: 20156821
coevolution; food handling; masting; scatter hoarding; seed dispersal; species interactions
21.  Large-Scale Genetic Structuring of a Widely Distributed Carnivore - The Eurasian Lynx (Lynx lynx) 
PLoS ONE  2014;9(4):e93675.
Over the last decades the phylogeography and genetic structure of a multitude of species inhabiting Europe and North America have been described. The flora and fauna of the vast landmasses of north-eastern Eurasia are still largely unexplored in this respect. The Eurasian lynx is a large felid that is relatively abundant over much of the Russian sub-continent and the adjoining countries. Analyzing 148 museum specimens collected throughout its range over the last 150 years we have described the large-scale genetic structuring in this highly mobile species. We have investigated the spatial genetic patterns using mitochondrial DNA sequences (D-loop and cytochrome b) and 11 microsatellite loci, and describe three phylogenetic clades and a clear structuring along an east-west gradient. The most likely scenario is that the contemporary Eurasian lynx populations originated in central Asia and that parts of Europe were inhabited by lynx during the Pleistocene. After the Last Glacial Maximum (LGM) range expansions lead to colonization of north-western Siberia and Scandinavia from the Caucasus and north-eastern Siberia from a refugium further east. No evidence of a Berinigan refugium could be detected in our data. We observed restricted gene flow and suggest that future studies of the Eurasian lynx explore to what extent the contemporary population structure may be explained by ecological variables.
doi:10.1371/journal.pone.0093675
PMCID: PMC3973550  PMID: 24695745
22.  Dissecting the Within-Africa Ancestry of Populations of African Descent in the Americas 
PLoS ONE  2011;6(1):e14495.
Background
The ancestry of African-descended Americans is known to be drawn from three distinct populations: African, European, and Native American. While many studies consider this continental admixture, few account for the genetically distinct sources of ancestry within Africa – the continent with the highest genetic variation. Here, we dissect the within-Africa genetic ancestry of various populations of the Americas self-identified as having primarily African ancestry using uniparentally inherited mitochondrial DNA.
Methods and Principal Findings
We first confirmed that our results obtained using uniparentally-derived group admixture estimates are correlated with the average autosomal-derived individual admixture estimates (hence are relevant to genomic ancestry) by assessing continental admixture using both types of markers (mtDNA and Y-chromosome vs. ancestry informative markers). We then focused on the within-Africa maternal ancestry, mining our comprehensive database of published mtDNA variation (∼5800 individuals from 143 African populations) that helped us thoroughly dissect the African mtDNA pool. Using this well-defined African mtDNA variation, we quantified the relative contributions of maternal genetic ancestry from multiple W/WC/SW/SE (West to South East) African populations to the different pools of today's African-descended Americans of North and South America and the Caribbean.
Conclusions
Our analysis revealed that both continental admixture and within-Africa admixture may be critical to achieving an adequate understanding of the ancestry of African-descended Americans. While continental ancestry reflects gender-specific admixture processes influenced by different socio-historical practices in the Americas, the within-Africa maternal ancestry reflects the diverse colonial histories of the slave trade. We have confirmed that there is a genetic thread connecting Africa and the Americas, where each colonial system supplied their colonies in the Americas with slaves from African colonies they controlled or that were available for them at the time. This historical connection is reflected in different relative contributions from populations of W/WC/SW/SE Africa to geographically distinct Africa-derived populations of the Americas, adding to the complexity of genomic ancestry in groups ostensibly united by the same demographic label.
doi:10.1371/journal.pone.0014495
PMCID: PMC3017210  PMID: 21253579
23.  Physiological mechanisms for food-hoarding motivation in animals 
The study of ingestive behaviour has an extensive history, starting as early as 1918 when Wallace Craig, an animal behaviourist, coined the terms ‘appetitive’ and ‘consummatory’ for the two-part sequence of eating, drinking and sexual behaviours. Since then, most ingestive behaviour research has focused on the neuroendocrine control of food ingestion (consummatory behaviour). The quantity of food eaten, however, is also influenced by the drive both to acquire and to store food (appetitive behaviour). For example, hamster species have a natural proclivity to hoard food and preferentially alter appetitive ingestive behaviours in response to environmental changes and/or metabolic hormones and neuropeptides, whereas other species would instead primarily increase their food intake. Therefore, with the strong appetitive component to their ingestive behaviour that is relatively separate from their consummatory behaviour, they seem an ideal model for elucidating the neuroendocrine mechanisms underlying the control of food hoarding and foraging. This review focuses on the appetitive side of ingestive behaviour, in particular food hoarding, attempting to integrate what is known about the neuroendocrine mechanisms regulating this relatively poorly studied behaviour. An hypothesis is formed stating that the direction of ‘energy flux’ is a unifying factor for the control of food hoarding.
doi:10.1098/rstb.2009.0225
PMCID: PMC2830250  PMID: 20156819
ingestive behaviour; energy balance; hoarding; appetitive behaviour; food intake; foraging
24.  Body mass loss during adaptation to short winter-like days increases food foraging, but not food hoarding 
Physiology & behavior  2009;97(1):135-140.
Siberian hamsters markedly reduce their body/lipid mass (~20–45%) in short ‘winter-like’ days (SD). Decreases in body/lipid mass associated with food deprivation or lipectomy result in increases in foraging and food hoarding. When at their SD-induced body/lipid mass nadir, food hoarding is not increased despite their decreases in body/lipid mass, but hoarding was not tested during the dynamic period of body/lipid mass loss (first 5–6 weeks of SDs). Therefore, we tested for changes in foraging/hoarding during this initial period in Siberian hamsters housed in a simulated burrow with a wheel running-based foraging system and exposed to either long ‘summer-like’ days (LD) or SDs. Two foraging effort conditions were used: 10 Revolutions/Pellet (pellet delivered after running 10 revolutions) and a Free Wheel/Free Food condition (wheel available, food pellets non-contingently available). Regardless of the foraging condition, body mass was significantly reduced across 8 weeks of SDs (~ 15%). Foraging increased after 7 weeks in SDs, but food hoarding did not increase compared to LDs. Instead food hoarding significantly decreased in SDs at Weeks 2–5 compared with Week 0 values, with the 10 Revolutions/Pellet foraging group returning to LD levels thereafter and the Free Wheel/Free Food group remaining reduced from Weeks 0–8. Collectively, we found that SDs decreased body mass, increased foraging after 7 weeks, and increased food hoarding, but only after an initial decrease and not above that seen in LDs. These data suggest that SD-induced body/lipid mass losses do not engender similar behavioral responses as seen with food deprivation or lipectomy.
doi:10.1016/j.physbeh.2009.02.012
PMCID: PMC2662045  PMID: 19224707
Siberian hamsters; hamsters; seasonal; appetitive behaviors; wheel running
25.  MTII attenuates ghrelin- and food deprivation-induced increases in food hoarding and food intake 1 
Hormones and behavior  2007;52(5):612-620.
Food deprivation triggers a constellation of physiological and behavioral changes including increases in peripherally-produced ghrelin and centrally-produced agouti-related protein (AgRP). Upon refeeding, food intake is increased in most species, however hamsters primarily increase food hoarding. Food deprivation-induced increases in food hoarding by Siberian hamsters are mimicked by peripheral ghrelin and central AgRP injections. Because food deprivation stimulates ghrelin as well as AgRP synthesis/release, food deprivation-induced increases in hoarding may be mediated by melanocortin 3 or 4 receptor (MC3/4-R) antagonism via AgRP, the MC3/4-R inverse agonist. Therefore, we asked: Can a MC3/4-R agonist block food deprivation- or ghrelin-induced increases in foraging, food hoarding and food intake? This was accomplished by injecting melanotan II (MTII), a synthetic MC3/4-R agonist, into the 3rd ventricle in food deprived, fed or peripheral ghrelin injected hamsters and housed in a running wheel-based food delivery foraging system. Three foraging conditions were used: a) no running wheel access, non-contingent food, b) running wheel access, non-contingent or c) a foraging requirement for food (10 revolutions/pellet). Food deprivation was a more potent stimulator of foraging and hoarding than ghrelin. Concurrent injections of MTII completely blocked food deprivation- and ghrelin-induced increases in food intake and attenuated, but did not always completely block, food deprivation- and ghrelin-induced increases in food hoarding. Collectively, these data suggest that the MC3/4-R are involved in ghrelin- and food deprivation-induced increases in food intake, but other neurochemical systems, such as previously demonstrated with neuropeptide Y, also are involved in increases in food hoarding as well as foraging.
doi:10.1016/j.yhbeh.2007.07.014
PMCID: PMC2121140  PMID: 17826779
fasting; foraging; melanotan II; hamster; Siberian hamster; intracerebroventricular

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