Extinct Beringian wolf morphotype found in the continental U.S. has implications for wolf migration and evolution

Pleistocene diversity was much higher than today, for example there were three distinct wolf morphotypes (dire, gray, Beringian) in North America versus one today (gray). Previous fossil evidence suggested that these three groups overlapped ecologically, but split the landscape geographically. The Natural Trap Cave (NTC) fossil site in Wyoming, USA is an ideally placed late Pleistocene site to study the geographical movement of species from northern to middle North America before, during, and after the last glacial maximum. Until now, it has been unclear what type of wolf was present at NTC. We analyzed morphometrics of three wolf groups (dire, extant North American gray, Alaskan Beringian) to determine which wolves were present at NTC and what this indicates about wolf diversity and migration in Pleistocene North America. Results show NTC wolves group with Alaskan Beringian wolves. This provides the first morphological evidence for Beringian wolves in mid‐continental North America. Their location at NTC and their radiocarbon ages suggest that they followed a temporary channel through the glaciers. Results suggest high levels of competition and diversity in Pleistocene North American wolves. The presence of mid‐continental Beringian morphotypes adds important data for untangling the history of immigration and evolution of Canis in North America.     

Y‐chromosome evidence supports widespread signatures of three‐species Canis hybridization in eastern North America

There has been considerable discussion on the origin of the red wolf and eastern wolf and their evolution independent of the gray wolf. We analyzed mitochondrial DNA (mtDNA) and a Y‐chromosome intron sequence in combination with Y‐chromosome microsatellites from wolves and coyotes within the range of extensive wolf–coyote hybridization, that is, eastern North America. The detection of divergent Y‐chromosome haplotypes in the historic range of the eastern wolf is concordant with earlier mtDNA findings, and the absence of these haplotypes in western coyotes supports the existence of the North American evolved eastern wolf (Canis lycaon). Having haplotypes observed exclusively in eastern North America as a result of insufficient sampling in the historic range of the coyote or that these lineages subsequently went extinct in western geographies is unlikely given that eastern‐specific mtDNA and Y‐chromosome haplotypes represent lineages divergent from those observed in extant western coyotes. By combining Y‐chromosome and mtDNA distributional patterns, we identified hybrid genomes of eastern wolf, coyote, gray wolf, and potentially dog origin in Canis populations of central and eastern North America. The natural contemporary eastern Canis populations represent an important example of widespread introgression resulting in hybrid genomes across the original C. lycaon range that appears to be facilitated by the eastern wolf acting as a conduit for hybridization. Applying conventional taxonomic nomenclature and species‐based conservation initiatives, particularly in human‐modified landscapes, may be counterproductive to the effective management of these hybrids and fails to consider their evolutionary potential.     

INTROGRESSION OF COYOTE MITOCHONDRIAL DNA INTO SYMPATRIC NORTH AMERICAN GRAY WOLF POPULATIONS

Mitochondrial DNA (mtDNA) genotypes of gray wolves and coyotes from localities throughout North America were determined using restriction fragment length polymorphisms. Of the 13 genotypes found among the wolves, 7 are clearly of coyote origin, indicating that genetic transfer of coyote mtDNA into wolf populations has occurred through hybridization. The transfer of mtDNA appears unidirectional from coyotes into wolves because no coyotes sampled have a wolf-derived mtDNA genotype. Wolves possessing coyote-derived genotypes are confined to a contiguous geographic region in Minnesota, Ontario, and Quebec, and the frequency of coyote-type mtDNA in these wolf populations is high (>50%). The ecological history of the hybrid zone suggests that hybridization is taking place in regions where coyotes have only recently become abundant following conversion of forests to farmlands. Dispersing male wolves unable to find conspecific mates may be pairing with female coyotes in deforested areas bordering wolf territories. Our results demonstrate that closely related species of mobile terrestrial vertebrates have the potential for extensive genetic exchange when ecological conditions change suddenly.     

周口店变异狼(Canis lupus variabilis)在家畜狗(Canis familiaris)祖先系列中的位置

本文作者对周口店第一、第三及第十三地点的一种化石犬类——变异狼(Canis lupus uariadilis)进行了观察和测量。根据其头骨大小、形态特征以及与中国早期人类共生的情况来看,认为它有可能是从驯化的野生狼导致家畜狗出现的一种祖先类型。     

Reviving the African Wolf Canis lupus lupaster in North and West Africa: A Mitochondrial Lineage Ranging More than 6,000 km Wide

The recent discovery of a lineage of gray wolf in North-East Africa suggests the presence of a cryptic canid on the continent, the African wolf Canis lupus lupaster. We analyzed the mtDNA diversity (cytochrome b and control region) of a series of African Canis including wolf-like animals from North and West Africa. Our objectives were to assess the actual range of C. l. lupaster, to further estimate the genetic characteristics and demographic history of its lineage, and to question its taxonomic delineation from the golden jackal C. aureus, with which it has been considered synonymous. We confirmed the existence of four distinct lineages within the gray wolf, including C. lupus/familiaris (Holarctic wolves and dogs), C. l. pallipes, C. l. chanco and C. l. lupaster. Taxonomic assignment procedures identified wolf-like individuals from Algeria, Mali and Senegal, as belonging to C. l. lupaster, expanding its known distribution c. 6,000 km to the west. We estimated that the African wolf lineage (i) had the highest level of genetic diversity within C. lupus, (ii) coalesced during the Late Pleistocene, contemporaneously with Holarctic wolves and dogs, and (iii) had an effective population size of c. 80,000 females. Our results suggest that the African wolf is a relatively ancient gray wolf lineage with a fairly large, past effective population size, as also suggested by the Pleistocene fossil record. Unique field observations in Senegal allowed us to provide a morphological and behavioral diagnosis of the African wolf that clearly distinguished it from the sympatric golden jackal. However, the detection of C. l. lupaster mtDNA haplotypes in C. aureus from Senegal brings the delineation between the African wolf and the golden jackal into question. In terms of conservation, it appears urgent to further characterize the status of the African wolf with regard to the African golden jackal.     

RAD sequencing and genomic simulations resolve hybrid origins within North American Canis

Top predators are disappearing worldwide, significantly changing ecosystems that depend on top-down regulation. Conflict with humans remains the primary roadblock for large carnivore conservation, but for the eastern wolf (Canis lycaon), disagreement over its evolutionary origins presents a significant barrier to conservation in Canada and has impeded protection for grey wolves (Canis lupus) in the USA. Here, we use 127 235 single-nucleotide polymorphisms (SNPs) identified from restriction-site associated DNA sequencing (RAD-seq) of wolves and coyotes, in combination with genomic simulations, to test hypotheses of hybrid origins of Canis types in eastern North America. A principal components analysis revealed no evidence to support eastern wolves, or any other Canis type, as the product of grey wolf × western coyote hybridization. In contrast, simulations that included eastern wolves as a distinct taxon clarified the hybrid origins of Great Lakes-boreal wolves and eastern coyotes. Our results support the eastern wolf as a distinct genomic cluster in North America and help resolve hybrid origins of Great Lakes wolves and eastern coyotes. The data provide timely information that will shed new light on the debate over wolf conservation in eastern North America.     

Human influence on distribution and extinctions of the late Pleistocene Eurasian megafauna

Late Pleistocene extinctions are of interest to paleontological and anthropological research. In North America and Australia, human occupation occurred during a short period of time and overexploitation may have led to the extinction of mammalian megafauna. In northern Eurasia megafaunal extinctions are believed to have occurred over a relatively longer period of time, perhaps as a result of changing environmental conditions, but the picture is much less clear. To consider megafaunal extinction in Eurasia, we compare differences in the geographical distribution and commonness of extinct and extant species between paleontological and archaeological localities from the late middle Pleistocene to Holocene. Purely paleontological localities, as well as most extinct species, were distributed north of archaeological sites and of the extant species, suggesting that apart from possible differences in adaptations between humans and other species, humans could also have a detrimental effect on large mammal distribution. However, evidence for human overexploitation applies only to the extinct steppe bison Bison priscus. Other human-preferred species survive into the Holocene, including Rangifer tarandus, Equus ferus, Capreolus capreolus, Cervus elaphus, Equus hemionus, Saiga tatarica, and Sus scrofa. Mammuthus primigenius and Megaloceros giganteus were rare in archaeological sites. Carnivores appear little influenced by human presence, although they become rarer in Holocene archaeological sites. Overall, the data are consistent with the conclusion that humans acted as efficient hunters selecting for the most abundant species. Our study supports the idea that the late Pleistocene extinctions were environmentally driven by climatic changes that triggered habitat fragmentation, species range reduction, and population decrease, after which human interference either by direct hunting or via indirect activities probably became critical.     

Biotic responses of canids to the terminal Pleistocene megafauna extinction

Trophic downgrading is a major concern for conservation scientists. The largest consumers in many ecosystems have become either rare or extirpated, leading to worry over the loss of their ecosystem function. However, trophic downgrading is not a uniquely modern phenomenon. The extinction of 34 genera of megafauna from North America ～13 000 yr ago must have led to widespread changes in terrestrial ecosystem function. Studies that have examined the event address impacts on vegetative structure, small mammal communities, nutrient cycling, and fire regimes. Relatively little attention has been paid to community changes at the top of the food chain. Here, we examine the response of carnivores in North America to the Pleistocene extinction. We employ fossil data to model the climatic niche of endemic canids, including the extinct dire wolf Canis dirus, over the last 20 000 yr. Quantifying the abiotic niche allows us to account for expected changes due to climate fluctuations over the Late Quaternary; deviations from expected responses likely reveal influences of competition and/or resource availability. We quantify the degree of niche conservatism and interspecific overlap to assess species and community responses among canids. We also include in our analyses a novel introduced predator, the domestic dog Canis lupus familiaris, which accompanied humans into the New World. We find that endemic canid species display low fidelity to their climatic niche through time, We find that survivors increasingly partition their climatic niche throughout the Holocene and, surprisingly, do not expand into niche space presumably vacated by the extinction of very large carnivores. These results suggest that loss of megaherbivores and competition with humans likely outweighed advantages conferred from the loss of very large predators. We also find that wolves and dogs decrease their niche overlap throughout the Holocene, suggesting a distinctive relationship between dogs and man.     

Canid hybridization: contemporary evolution in human‐modified landscapes

Contemporary evolution through human‐induced hybridization occurs throughout the taxonomic range. Formerly allopatric species appear especially susceptible to hybridization. Consequently, hybridization is expected to be more common in regions with recent sympatry owing to human activity than in areas of historical range overlap. Coyotes ( Canis latrans) and gray wolves ( C. lupus) are historically sympatric in western North America. Following European settlement gray wolf range contracted, whereas coyote range expanded to include eastern North America. Furthermore, wolves with New World (NW) mitochondrial DNA (mtDNA) haplotypes now extend from Manitoba to Québec in Canada and hybridize with gray wolves and coyotes. Using mtDNA and 12 microsatellite markers, we evaluated levels of wolf‐coyote hybridization in regions where coyotes were present (the Canadian Prairies, n = 109 samples) and absent historically (Québec, n = 154). Wolves with NW mtDNA extended from central Saskatchewan (51°N, 69°W) to northeastern Québec (54°N, 108°W). On the Prairies, 6.3% of coyotes and 9.2% of wolves had genetic profiles suggesting wolf‐coyote hybridization. In contrast, 12.6% of coyotes and 37.4% of wolves in Québec had profiles indicating hybrid origin. Wolves with NW and Old World ( C. lupus) mtDNA appear to form integrated populations in both regions. Our results suggest that hybridization is more frequent in historically allopatric populations. Range shifts, now expected across taxa following climate change and other human influence on the environment, might therefore promote contemporary evolution by hybridization.     

A new mitochondrial haplotype confirms the distinctiveness of the Italian wolf (Canis lupus) population

In the past century the Italian wolf has been repeatedly indicated as a distinct subspecies, Canis lupus italicus, due to its unique morphology and its distinctive mtDNA control region (CR) monomorphism. However, recent studies on wolf x dog hybridization in Italy documented the presence of a second mtDNA CR haplotype (W16), previously found only in wolves from Eastern Europe, casting doubts on the genetic uniqueness of the Italian wolves. To test whether this second haplotype belongs to the Italian wolf population, we genotyped 92 wolf DNA samples from Italy, Slovenia, Greece and Bulgaria at four mtDNA regions (control-region, ATP6, COIII and ND4 genes) and at 39 autosomal microsatellites. Results confirm the presence of two mtDNA multi-fragment haplotypes (WH14 and WH19) in the Italian wolves, distinct from all the other European wolves. Network analyses of the multi-fragment mtDNA haplotypes identified two strongly differentiated clades, with the Italian wolf WH14 and WH19 multi-fragment haplotypes rooted together. Finally, Bayesian clustering clearly assigned all the wolves sampled in Italy to the Italian population, regardless of the two different multi-fragment haplotypes. These results demonstrate that the W16 CR haplotype is part of the genetic pool of the Italian wolf population, reconfirming its distinctiveness from other European wolves. Overall, considering the presence of unique mtDNA and Y-linked haplotypes, the sharply different frequencies of genome-wide autosomal alleles and the distinct morphological features of Italian wolves, we believe that this population should be considered a distinct subspecies.     

Analysis of <Emphasis Type="Italic">Canis</Emphasis> mitochondrial DNA demonstrates high concordance between the control region and ATPase genes

Background  

Phylogenetic studies of wild Canis species have relied heavily on the mitochondrial DNA control region (mtDNA CR) to infer species relationships and evolutionary lineages. Previous analyses of the CR provided evidence for a North American evolved eastern wolf (C. lycaon), that is more closely related to red wolves (C. rufus) and coyotes (C. latrans) than grey wolves (C. lupus). Eastern wolf origins, however, continue to be questioned. Therefore, we analyzed mtDNA from 89 wolves and coyotes across North America and Eurasia at 347 base pairs (bp) of the CR and 1067 bp that included the ATPase6 and ATPase8 genes. Phylogenies and divergence estimates were used to clarify the evolutionary history of eastern wolves, and regional comparisons of nonsynonomous to synonomous substitutions (dN/dS) at the ATPase6 and ATPase8 genes were used to elucidate the potential role of selection in shaping mtDNA geographic distribution.     

Wolves in the Great Lakes region: a phylogeographic puzzle

Empirical studies demonstrate that natural hybridization in animals is more common than thought so far ( Mallet 2005 ), particularly among species that originated recently through cycles of population contraction–expansion arising from climate changes over the last glacial period, the Pleistocene. In addition, the post‐glacial global growth of human populations has fostered anthropogenic hybridization events, mediated by habitat changes, the persecution of large predators and the introduction of alien species ( Allendorf et al. 2001 ). The Canis lineage shows cases of both natural and anthropogenic hybridization, exacerbating the controversy about the number of species that should be formally validated in the taxonomic lists, the evolutionary role of genetic introgression and the ways to manage hybrids with invading wild or domesticated populations. The study by Wheeldon et al. (2010) , published in this issue of Molecular Ecology, adds a new piece to the intricate puzzle of evolution and taxonomy of Canis in North America. They show that sympatric wolves (C. lupus) and coyotes (C. latrans) are not (extensively) hybridizing in the western North American Great Lakes region (GLR). Widespread hybridization between coyotes and a genetically distinct, but closely related, wolf‐like population (the eastern wolf) occurred in the northeastern regions of North America. In Wheeldon et al.’s (2010) opinion, these data should prove definitely that two different species of wolf (the western gray wolf C. lupus and the eastern wolf C. lycaon) and their hybrids are distributed across the GLR.     

Going coastal: shared evolutionary history between coastal British Columbia and Southeast Alaska wolves (Canis lupus)

Background

Many coastal species occupying the temperate rainforests of the Pacific Northwest in North America comprise endemic populations genetically and ecologically distinct from interior continental conspecifics. Morphological variation previously identified among wolf populations resulted in recognition of multiple subspecies of wolves in the Pacific Northwest. Recently, separate genetic studies have identified diverged populations of wolves in coastal British Columbia and coastal Southeast Alaska, providing support for hypotheses of distinct coastal subspecies. These two regions are geographically and ecologically contiguous, however, there is no comprehensive analysis across all wolf populations in this coastal rainforest.

Methodology/Principal Findings

By combining mitochondrial DNA datasets from throughout the Pacific Northwest, we examined the genetic relationship between coastal British Columbia and Southeast Alaska wolf populations and compared them with adjacent continental populations. Phylogenetic analysis indicates complete overlap in the genetic diversity of coastal British Columbia and Southeast Alaska wolves, but these populations are distinct from interior continental wolves. Analyses of molecular variation support the separation of all coastal wolves in a group divergent from continental populations, as predicted based on hypothesized subspecies designations. Two novel haplotypes also were uncovered in a newly assayed continental population of interior Alaska wolves.

Conclusions/Significance

We found evidence that coastal wolves endemic to these temperate rainforests are diverged from neighbouring, interior continental wolves; a finding that necessitates new international strategies associated with the management of this species.     

Ancient DNA suggests modern wolves trace their origin to a Late Pleistocene expansion from Beringia

Grey wolves (Canis lupus) are one of the few large terrestrial carnivores that have maintained a wide geographical distribution across the Northern Hemisphere throughout the Pleistocene and Holocene. Recent genetic studies have suggested that, despite this continuous presence, major demographic changes occurred in wolf populations between the Late Pleistocene and early Holocene, and that extant wolves trace their ancestry to a single Late Pleistocene population. Both the geographical origin of this ancestral population and how it became widespread remain unknown. Here, we used a spatially and temporally explicit modelling framework to analyse a data set of 90 modern and 45 ancient mitochondrial wolf genomes from across the Northern Hemisphere, spanning the last 50,000 years. Our results suggest that contemporary wolf populations trace their ancestry to an expansion from Beringia at the end of the Last Glacial Maximum, and that this process was most likely driven by Late Pleistocene ecological fluctuations that occurred across the Northern Hemisphere. This study provides direct ancient genetic evidence that long‐range migration has played an important role in the population history of a large carnivore, and provides insight into how wolves survived the wave of megafaunal extinctions at the end of the last glaciation. Moreover, because Late Pleistocene grey wolves were the likely source from which all modern dogs trace their origins, the demographic history described in this study has fundamental implications for understanding the geographical origin of the dog.     

中国狼不同地理种群遗传多样性及系统进化分析

为了解中国狼不同地理种群遗传多样性及系统发育情况,从中国境内狼的主要分布区青海、新疆、内蒙古和吉林4个地区采集样品,用分子生物学技术手段成功地获得44个个体线粒体DNA控制区第一高变区(HVRⅠ)序列和40个线粒体Cyt b部分序列。线粒体控制区HVRⅠ共检测到51个变异位点,位点变异率为8.76%;线粒体Cyt b部分序列发现31个变异位点,位点变异率为5.33%,未见插入及缺失现象,变异类型全部为碱基置换。共定义了16个线粒体HVRⅠ单倍型,其中吉林与内蒙种群存在共享单倍型,估计这两地间种群亲缘关系较近。4个地理种群中新疆种群拥有较高的遗传多样性(0.94)。中国狼种群总体平均核苷酸多态性为2.27%,与世界其他国家地区相比,中国狼种群拥有相对较高的遗传多样性。通过线粒体HVRⅠ单倍型构建的系统进化树可以看出,中国狼在进化上分为2大支,其中位于青藏高原的青海种群独立为一支,推测其可能长期作为独立种群进化。基于青海种群与新疆,内蒙种群的线粒体Cyt b遗传距离,推测中国狼2个世系可能在更新世冰川时期青藏高原受地质作用急速隆起后出现分歧,分歧时间大约在1.1 MY前。     

Phylogenetic relationships among Palearctic and Nearctic burbot (Lota lota): Pleistocene extinctions and recolonization

The burbot (Lota lota Linnaeus, 1758) is the only freshwater species from the cod family. Various taxonomic hypotheses were tested against molecular data by sequencing the mitochondrial cytochrome b locus of 120 burbot from 41 populations together with the related species Molva molva (ling) and Brosme brosme (tusk), which represented the other Lotinae genera. Within the genus Lota two distinct phylogroups were observed: one in North America south of the Great Slave Lakes (Lota lota maculosa) and one in Eurasia and the remainder of the Nearctic region (Lota lota lota). The burbot lineage separated 10 Myr BP from the other Lotinae, while the genetic variation within burbot appeared to be approximately 1 Myr old. However, fossil evidence suggested that burbot already existed in the Early Pliocene in Europe, from were it probably colonized North America in the Early Pleistocene. While Nearctic burbot survived climatic oscillations and diverged in several refugia, the Eurasian form became extinct or was reduced to a very small population. In the Late Pleistocene the species recolonized the Palearctic region to establish its present distribution range.     

Genetic and morphometric analysis of sixteenth century <Emphasis Type="Italic">Canis</Emphasis> skull fragments: implications for historic eastern and gray wolf distribution in North America

Resolving the taxonomy and historic ranges of species are essential to recovery plans for species at risk and conservation programs that aim to restore extirpated populations. In eastern North America, planning for wolf population restoration is complicated by the disputed historic distributions of two wolf species: the Old World-evolved gray wolf (Canis lupus) and the New World-evolved eastern wolf (C. lycaon). We used genetic and morphometric data from 4- to 500-year-old Canis samples excavated in London, Ontario, Canada to help clarify the historic range of these two wolf species in the eastern temperate forests of North America. We isolated DNA and sequenced the mitochondrial control region and found that none of the samples were of gray wolf origin. Two of the DNA sequences corresponded to those found in present day coyotes (C. latrans), but morphometric comparisons show an eastern wolf, not coyote, origin. The remaining two sequences matched ancient domestic dog haplotypes. These results suggest that the New World-evolved eastern wolf, not the gray wolf, occupied this region prior to the arrival of European settlers, although eastern-gray wolf hybrids cannot be ruled out. Furthermore, our data support the idea of a shared common ancestry between eastern wolves and western coyotes, and that the distribution of gray wolves at this time probably did not include the eastern temperate forests of North America.     

Historical and ecological determinants of genetic structure in arctic canids

Wolves (Canis lupus) and arctic foxes (Alopex lagopus) are the only canid species found throughout the mainland tundra and arctic islands of North America. Contrasting evolutionary histories, and the contemporary ecology of each species, have combined to produce their divergent population genetic characteristics. Arctic foxes are more variable than wolves, and both island and mainland fox populations possess similarly high microsatellite variation. These differences result from larger effective population sizes in arctic foxes, and the fact that, unlike wolves, foxes were not isolated in discrete refugia during the Pleistocene. Despite the large physical distances and distinct ecotypes represented, a single, panmictic population of arctic foxes was found which spans the Svalbard Archipelago and the North American range of the species. This pattern likely reflects both the absence of historical population bottlenecks and current, high levels of gene flow following frequent long-distance foraging movements. In contrast, genetic structure in wolves correlates strongly to transitions in habitat type, and is probably determined by natal habitat-biased dispersal. Nonrandom dispersal may be cued by relative levels of vegetation cover between tundra and forest habitats, but especially by wolf prey specialization on ungulate species of familiar type and behaviour (sedentary or migratory). Results presented here suggest that, through its influence on sea ice, vegetation, prey dynamics and distribution, continued arctic climate change may have effects as dramatic as those of the Pleistocene on the genetic structure of arctic canid species.     

Differentiation of tundra/taiga and boreal coniferous forest wolves: genetics, coat colour and association with migratory caribou

The grey wolf has one of the largest historic distributions of any terrestrial mammal and can disperse over great distances across imposing topographic barriers. As a result, geographical distance and physical obstacles to dispersal may not be consequential factors in the evolutionary divergence of wolf populations. However, recent studies suggest ecological features can constrain gene flow. We tested whether wolf-prey associations in uninterrupted tundra and forested regions of Canada explained differences in migratory behaviour, genetics, and coat colour of wolves. Satellite-telemetry data demonstrated that tundra wolves (n = 19) migrate annually with caribou (n = 19) from denning areas in the tundra to wintering areas south of the treeline. In contrast, nearby boreal coniferous forest wolves are territorial and associated year round with resident prey. Spatially explicit analysis of 14 autosomal microsatellite loci (n = 404 individuals) found two genetic clusters corresponding to tundra vs. boreal coniferous forest wolves. A sex bias in gene flow was inferred based on higher levels of mtDNA divergence (F(ST) = 0.282, 0.028 and 0.033; P < 0.0001 for mitochondrial, nuclear autosomal and Y-chromosome markers, respectively). Phenotypic differentiation was substantial as 93% of wolves from tundra populations exhibited light colouration whereas only 38% of boreal coniferous forest wolves did (chi(2) = 64.52, P < 0.0001). The sharp boundary representing this discontinuity was the southern limit of the caribou migration. These findings show that substantial genetic and phenotypic differentiation in highly mobile mammals can be caused by prey-habitat specialization rather than distance or topographic barriers. The presence of a distinct wolf ecotype in the tundra of North America highlights the need to preserve migratory populations.     

Megafauna extinction,tree species range reduction,and carbon storage in Amazonian forests

During the Late Pleistocene and early Holocene 59 species of South American megafauna went extinct. Their extinction potentially triggered population declines of large‐seeded tree species dispersed by the large‐bodied frugivores with which they co‐evolved, a theory first proposed by Janzen and Martin (1982). We tested this hypothesis using species range maps for 257 South American tree species, comparing 63 species thought to be primarily distributed by megafauna with 194 distributed by other animals. We found a highly significant (p < 0.001) decreased mean range size of 26% for the megafauna dispersed fruit (n = 63 species) versus fruit dispersed by other animals (n = 194), results which support the hypothesis. We then developed a mathematical model of seed dispersal to estimate the theoretical impact of megafauna extinction on tree species range and found the estimated dispersal capacity (Φ_seed) of a 2 g seed decreases by > 95% following disperser extinction. A numerical gap dynamic simulations suggests that over a 10 000 yr period following the disperser extinctions, the average convex hull range size of large‐seeded tree species decreased by ～ 31%, while the estimated decrease in population size was ～ 54%, indicating a likely greater decrease in species population size than indicated by the empirical range patterns. Finally, we found a positive correlation between seed size and wood density of animal‐dispersed tree species implying that the Late Pleistocene and early Holocene megafaunal extinctions reduced carbon content in the Amazon by ～ 1.5 ± 0.7%. In conclusion, we 1) provide some empirical evidence that megafauna distributed fruit species have a smaller mean range size than wind, water or other animal‐dispersed species, 2) demonstrate mathematically that such range reductions are expected from megafauna extinctions ca 12 000 yr ago, and 3) illustrate that these extinctions may have reduced the Amazon's carbon storage capacity.