Analyses of mitochondrial and microsatellite data, however, estimated that the common ancestor of North American pumas lived within the last 20, years 7 , 8 and that the genetic diversity of all modern pumas traces to eastern South America 7. The combination of genetic and fossil data were interpreted as reflecting a North American origin of the puma lineage followed by local extinction in North America during the late Pleistocene and subsequent recolonization from South America as the climate warmed after the last ice age 7 , 8.
Recently, however, an unequivocal puma fossil was discovered in Argentina that dates to 1. This discovery pushes back the age of the puma lineage by more than , years, and suggests that the ancestor of all living pumas may have evolved in South America rather than North America. During the 19th and 20th centuries, bounty hunting reduced, and in some cases extirpated, puma populations across North America 10 , restricting them to the North American West and the southern tip of Florida.
By the middle of the 20th century, hunting quotas and some outright bans 12 allowed puma populations to increase and recolonize parts of their former range. Although some puma populations today are large and well-connected 13 , others are small and fragmented e.
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Many populations are experiencing increased isolation with the expansion of highways, residential developments, and agriculture 14 , Puma range past and present. The current range of pumas hashed compared to their historic range blue. Circles denote the geographic coordinates of the puma populations sampled in this study.
Panels show zoom-ins of puma habitat distribution dark gray within the known range of the species in the contiguous United States as predicted by the USGS Historic range data are approximated based on prior reports Base map generated with Natural Earth. The consequences of geographic isolation on puma genetic diversity and fitness have been well documented, particularly in Florida, where they are a federally protected subspecies commonly called the Florida panther. By the s, the canonical Florida panther population in Big Cypress National Preserve was suffering from reproductive failure and phenotypic defects associated with inbreeding 16 , To rescue the Florida panthers from extinction, eight female pumas from Texas were released in South Florida in , of which five successfully produced offspring.
By , the occurrence of phenotypic defects had significantly declined, survival measures had improved, and the population size increased almost threefold 16 , All Florida panthers genotyped since show ancestry that includes admixture with the introduced lineages Florida panthers in Everglades National Park are partially isolated from the core canonical population that persisted in Big Cypress National Preserve by a semipermeable barrier associated with hydrologic fluctuations of the Everglades. Intriguingly, during the s, the Everglades panthers did not show the same high incidence of inbreeding-associated phenotypes as in the Big Cypress population.
The absence of observed phenotypic defects in the Everglades population may be attributable to the release during the s and s of captive-bred Florida panthers with mixed Central American ancestry into Everglades National Park. The admixed ancestry of the Everglades population and potential explanation for the reproductive success of the captive population was later discovered through genotyping Genetics has a long history as a tool in wildlife conservation In traditional conservation genetics, researchers sequence a small number of genetic markers across a large sampling of the species of interest.
Advances in sequencing technologies have made it possible to sequence whole genomes of non-model organisms, including species of conservation concern. While the cost of sequencing continues to decrease, sequencing whole genomes will undoubtedly remain more costly than sequencing only a handful of genetic loci.
This presents a choice: whole genome data sets exchange spatial resolution for finer-scale genomic resolution, allowing researchers to test different hypotheses. Each whole genome contains a multitude of largely-independent genealogies, which provides increased power to infer past events 23 , In particular, the dense haplotype information provided by whole genomes is necessary to examine the very short timescales 25 , 26 relevant to conservation efforts. Here, we reconstruct the last two million years of puma demographic history by generating and analyzing a draft genome from an individual sampled in the Santa Cruz Mountains California, USA , along with nine resequenced genomes from pumas from North and South America.
We confirm the recent maternal ancestry of North American pumas and describe genomic diversity in the sampled populations. We use shared tracts of homozygosity to predict the effectiveness of assisted gene flow in restoring lost genetic diversity. Finally, we analyze the genome of a Florida panther with admixed ancestry that was collected 30 years after the first release of Central American admixed pumas into the Everglades.
This genome allows us to assess the long-term efficacy of inter-population admixture as a means to rescue small and isolated populations from the deleterious effects of inbreeding. Our PumCon1. Although our ONT coverage was only 1. We produced three final call sets: the first containing 8 million variable sites using the 10 pumas, the second decreased to , variable sites after filtering the first call set for linkage disequilibrium LD , and the final call set containing , SNPs after LD filtering using the 10 pumas and the African cheetah see Methods section.
We reconstructed puma demographic history using both mitochondrial and nuclear genomes. The North American mitochondrial clade excludes the Florida Everglades puma EVG21 , which has a mitochondrial ancestry that is distinct from the rest of North America, consistent with the reported mixed ancestry of this individual Demographic history of pumas. We calculated divergence times by determining the number of pairwise divergences between sequences and used a mitochondrial divergence rate of 1. We assume a generation time of 5 years and a per generation mutation rate of 0.
The nuclear genomic data revealed a similar demographic history to that inferred from the mitochondrial data, and allowed us to estimate changes in effective population size over time. This increase may reflect an increase in numbers during colonization of unoccupied habitats in Central and North America, but may also be attributable to PSMC modeling overestimating effective population size when a species has divided into subpopulations To test whether this observed peak was the result of population structure, we modeled pseudo-diploid individuals using the X chromosomes of our male pumas see Methods section.
Thus, structure alone was not the reason behind the observed increase in N e during this time. The spike in effective population size observed for EVG21 probably does not reflect the coalescent process within a single population, but is instead consistent with mixed ancestry comprised of two divergent lineages We used the nuclear genomic data to characterize genetic structure among puma populations Fig.
Pumas sampled from the same population clustered together. Stratification of pumas based on the geographic population. The first component primarily separates South and North American pumas, while the second component distinguishes the variation within North America. We estimated a consensus nuclear phylogeny from , SNPs from the LD-filtered data set that included ten pumas and the African cheetah. This analysis found further evidence of structure, with the highest likelihood tree including a single migration event from a South or Central American lineage into the Everglades lineage Fig.
We note that the discrete populations identified in these analyses could simply reflect the spatial sampling of our data set. Spatially structured sampling can cause analyses to report distinct populations even when no discrete population structure exists This artifact is particularly likely to occur when geographically widespread samples are taken from well connected species where limited dispersal results in the accumulation of local genetic variants, resulting in genetic isolation by distance However, the observed geographic structure could also be the result of discrete genetic structure due to population isolation.
Some puma populations have experienced persecution and degradation of their habitat, resulting in limited gene flow between populations 16 , 34 , 35 , These isolated populations would show increased divergence over time, resulting in geographic structure. To examine the extent of inbreeding in our puma samples, we estimated for each individual average genome-wide heterozygosity and identified runs of homozygosity ROH across the 26 largest autosomal scaffolds Fig.
The distribution of ROH across the genome varied among scaffolds and individuals Fig. The two pumas from Brazil were the least inbred, with the highest heterozygosity and smallest proportions of their genomes in ROH. Conversely, the Big Cypress panthers sampled prior to the genetic rescue were the most inbred, with the lowest heterozygosity and the largest proportions of their genomes in ROH, consistent with the phenotypic defects recorded in these individuals The other North American pumas fell between these two extremes.
This is consistent with their origins, as genetic analysis suggests that SMM22 was likely born in the small and more isolated Santa Monica Mountains population south of US freeway, whereas SMM12 was first observed in the larger and more connected population north of US and dispersed into the Santa Monica Mountains as a subadult Heterozygosity and runs of homozygosity.
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Plots for all pumas are provided as Supplementary Fig. EVG21, the admixed Florida panther from the Everglades population, was an outlier in the general correlation between heterozygosity and proportion of the genome in ROH. This is consistent with both ancestral admixture resulting in a more diverse genetic background and close inbreeding leading to long tracts of homozygosity Supplementary Fig.
To better explore inbreeding history, we examined the distribution of ROH tract lengths in each puma. All North American pumas sampled had a large number of short ROH, indicating that these populations were small in the recent past 8—23 generations ago. The puma from Yellowstone had mostly short ROH and a small number of intermediate and long ROH, consistent with a population that was small in the recent past, but that does not suffer from a considerable amount of close inbreeding in recent generations. The pumas from the Santa Cruz and Santa Monica Mountains had patterns similar to the Yellowstone puma, except they had additional long ROH, suggesting that these populations are experiencing close inbreeding.
The Big Cypress panthers each had many long ROH, which we estimated to reflect shared ancestors within the last three generations. Long ROH that are also shared IBD between individuals are concerning because they represent regions of the genome with no genetic diversity in the four haplotypes analyzed.
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While most sampled North American populations show signs of close inbreeding, different populations are fixed for different variants and considerable genetic variation still exists when considering the species as a whole. We present a draft assembly of a puma genome, which we use to reconstruct the demographic history of the species and measure genome-wide heterozygosity and ROH, the latter of which is less practical with lower-quality or reference-guided genome assemblies.
Our analyses of ten complete puma genomes revealed the dynamic history of a once widespread species whose population size is now reduced across much of its range. Previously, the incomplete fossil record paired with divergence estimates based on rapidly evolving microsatellites and partial mitochondrial genomes led to the hypothesis of a North American origin of the species, followed by a late Pleistocene local extinction in North America and then a recolonization from South America within the last 20, years 7 , 8. Our results using complete nuclear and mitochondrial genomes are consistent with previous genetic analyses in that we show that North American pumas represent a subset of puma genetic diversity.
While we are unable to exclude the possibility of a local late Pleistocene extinction in North America followed by a recolonization from an unsampled lineage elsewhere in South or Central America, we argue that this nuclear genomic data in combination with a recently identified puma fossil in South America that dates to 1. We note that new fossils or genomic data from late Pleistocene aged pumas or pumas from other locations in South and Central America will be necessary to test this demographic hypothesis.
This hypothesis is supported by data from living pumas, which, despite a preference in North America for mountainous habitats, are also known to occupy grassland habitats in South America, such as Patagonia Differences in habitat selection between the two continents probably reflect a long history of competition with a diverse carnivore guild on both continents.
For example, jaguars are better adapted than pumas to living in habitats that flood periodically 41 , and predation by wolves in North America probably precludes pumas living in open habitat without escape terrain This period is associated with a reduction of available habitat across the continental United States, as the coalesced Laurentide and Cordilleran glaciers covered much of present-day Canada and the Upper Midwestern United States Forests would have been reduced significantly at that time, as would available habitat for the smaller prey preferred by pumas, providing a potential mechanism for a reduction in puma population size around that time.
The recent history of pumas is marked by human persecution and encroachment on their habitat, resulting in small and isolated populations that are susceptible to loss of genetic diversity and predisposed to inbreeding. Over many generations, without the input of novel variation from migrants, isolated populations can accumulate local genetic variation while losing overall genetic diversity.
Loss of genetic diversity may be a common situation for top predators, as their population densities are usually low and successful migrants are infrequent. Consequently, even moderate levels of fragmentation will affect their genomic diversity.
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While pumas in South America currently experience less habitat degradation than pumas in North America, pumas in South America will likely face further habitat loss and fragmentation as rapid human population growth and land development continues on the continent The result may be small, isolated populations in South America similar to those currently seen in North America.
Thus conservation efforts and findings taken from isolated populations in North America may need be applied in the future to other parts of the puma range. In North America, pumas were hunted extensively, resulting in low population densities in many areas of their range Hunting was so severe until regulations were put in place during the mid 20th century that pumas likely experienced a population bottleneck.
All North American pumas sampled in this study exhibit short ROH that date to approximately the early 20th century, indicative of small effective population sizes during the time when hunting was severe. In many areas of North America, including California and Florida, large-scale hunting was followed by shrinking habitat availability, resulting in small, isolated populations 15 , 44 , Our sampling focused on populations in North America that are known to be isolated and, as such, our results highlight the genomic consequences of this isolation—reduced diversity and signatures of close inbreeding.
This pattern is consistent with the known history of hunting and habitat availability in the Yellowstone area. Pumas in the Yellowstone area were hunted to low densities into the mid 20th century 10 , but today Yellowstone National Park is a large protected area surrounded by wildlands. This connectivity between the Park and wildlands facilitated the recovery and maintenance of genetic diversity in the local puma population once hunting pressures were reduced. Florida panthers are among the most well-studied populations of pumas, especially with regard to the phenotypic manifestations of isolation and inbreeding.
The introduction of pumas from Texas, the most geographically proximate population to the Florida panthers, is widely regarded as a successful genetic rescue via translocation. However, Florida panther genetic diversity in the Everglades population had been bolstered several decades earlier, when seven individuals were released into Everglades National Park from a captive facility where pumas from Central America had been included in the breeding population Her genome is a combination of regions with comparatively high heterozygosity, similar to that observed in the Brazilian pumas, and long ROH, similar to the highly inbred Florida panthers.
The distribution of the lengths of ROH suggest that her maternal and paternal lineages shared a common ancestor that lived shortly after the release of the admixed pumas into the Everglades population. This suggests that the genomic consequences of inbreeding happen quickly, with much of the gains from the genetic rescue being quickly erased.
Thus, a consistent effort is required to maintain the benefits of translocation. In many areas of the current puma range, human land use has reduced the connectivity that is critical to recovery and maintenance of healthy populations. Despite these barriers, gene flow among neighboring populations can be facilitated by enhancing landscape connectivity through coordinated land use planning and by adding bridges or underpasses across freeways Although pumas are capable of traveling long distances, large roads are a major barrier to their movement 14 , A model of population dynamics in the Santa Monica Mountains that incorporated landscape connectivity and its effects on genetic diversity predicted a high probability of extinction Our genomic analyses of the samples from the Santa Monica Mountains also support the effectiveness of population connectivity.
However SMM12 migrated into the subpopulation from north of US 15 , a larger area that shows greater connectivity to surrounding regions. Migrations between these two areas are now rare, but the two subpopulations were probably part of a larger panmictic population prior to the existence of US In contrast, individuals that originated from the same population have a much larger proportion of their genomes in IBD ROH e. This indicates that while inbreeding has reduced diversity in a considerable proportion of the genomes of individuals within small populations, these low diversity regions are generally not shared between populations.
Thus, reconnecting the populations on either side of US , as currently proposed via a wildlife crossing over the freeway, would help restore the lost genetic diversity. Genome-scale data sets have the potential to inform conservation planning. Our results highlight how whole genome data can provide new insights when compared to traditional conservation genetic techniques.
For instance, measures of average heterozygosity are the most commonly used metrics to characterize the genetic health of a species, as estimates are relatively simple to generate and are easily comparable among organisms. However, average heterozygosity provides only a narrow insight into the health and genetic potential of a species While in some species average genome-wide heterozygosity is highly correlated with the level of inbreeding estimated using ROH 26 , in systems with admixture, average heterozygosity estimates can be deceptive, as demonstrated with our admixed Everglades puma EVG We would infer two very different genetic conditions when considering each metric separately, and thus both heterozygosity and proportion of the genome in ROH should be considered in assessing genomic health.
Finally, knowledge of shared ROH, an analysis which can only be done with very high density markers across the genome, is critical when designing mitigation plans, as this analysis predicts whether enhancing connectivity would restore lost genetic diversity and helps identify potential candidates for translocation. In this context, this study can serve as a template for future conservation genomic research targeting species living in small, isolated populations.