Brief Population Bottlenecks Are Beyond The Genetic Streetlight

Inferring human demographic history from extant genomes is an important goal of population genetics. To date, the sensitivity of coalescence-based methods in detecting population bottlenecks has not been well characterized. In this study, we find that brief bottlenecks, of just a few generations, are undetectable by current methods. A new approach to population inference, Lineage Time Inference (LiTI), uses data-derived windows to demarcate the limits of the genetic data. We find that a sharp population bottleneck at the time of the Youngest Toba Eruption, and also at more ancient timepoints in the human lineage, would be outside the genetic streetlight.

Not out of the woods yet: signatures of the prolonged negative genetic consequences of a population bottleneck in a rapidly re-expanding wader, the black-faced spoonbill Platalea minor

The long-term persistence of a population which has suffered a bottleneck partly depends on how historical demographic dynamics impacted its genetic diversity and the accumulation of deleterious mutations. Here we provide genomic evidence for the detrimental genetic effect of a recent population bottleneck in the endangered black-faced spoonbill (Platalea minor) even after its rapid population recovery. Our population genomic data suggest that the bird’s effective population size, N, had been relatively stable (7,500-9,000) since the end of the last glacial maximum; however, a recent brief yet severe bottleneck (N= 20) around the 1940s wiped out more than 99% of its historical N in roughly three generations. By comparing it with its sister species, the royal spoonbill (P. regia) whose conservation status is of lesser concern, we found that despite a more than 15-fold population recovery since 1988, genetic drift has led to higher levels of inbreeding (7.4 times more runs of homozygosity longer than 100 Kb) in the black-faced spoonbill than in the royal spoonbill genome. Although the two spoonbills have similar levels of genome-wide nucleotide diversity and heterozygosity, because of relaxed purifying selection, individual black-faced spoonbills carry 3% more nonsynonymous substitutions than royal spoonbills each of which is 7% more deleterious. Our results imply that the persistence of a threatened species cannot be inferred from a recovery in its population. They also highlight the necessity of continually using genomic indices to monitor its genetic health and employing all possible measures to assure its long-term persistence in the ever-changing environment.

Impact of the Toba eruption on rainfall – a speleothem record suggests multi-staged eruption affected EASM

<p>The Toba eruption, marked by the Younger Toba Tuff (YTT), was the largest volcanic event of the Quaternary. Dated to 73.88±0.6 ka BP (2σ), this eruption must have been witnessed by humans globally, even if only through indirect effects of multi-year adverse weather patterns, or atmospheric phenomena. It has been proposed that the YTT acted as trigger or accelerator for Greenland Stadial 20 (GS20). Its global climatic impact is evidenced by data from as far as southwestern USA, Antarctica, and Greenland (Polyak et al. 2017, Svensson et al. 2013). Whether this event also caused a human population bottleneck (Ambrose 2003) remains debated (Petraglia et al. 2007, Ge et al. 2020).</p><p>Here we combine stable isotopes with laser ablation based multi-element data to test the impact of the YTT on the East Asian Summer Monsoon using a stalagmite from China.  U-series dating indicates that stalagmite XT5 grew between 87±0.3 to 50±0.4 ka BP. Oxygen and carbon isotope ratios show significant changes linked to GS20, with several large positive excursions between 74 and 70 ka BP suggesting severe droughts. The notion of severe drying is supported by the Sr profile. Several spikes in rare earth elements (REE: Y, La, Ce, Nd, Yb) occurred concurrent with δ<sup>18</sup>O, δ<sup>13</sup>C, and Sr increases.</p><p>The increasing δ<sup>13</sup>C and δ<sup>18</sup>O values resulted from reduced effective infiltration linked to a longer-term reorganization of the EASM system. The observed REE dynamics and can be interpreted as indicative of large eruption events. Assigning REE spikes to individual eruptions like the YTT remains ambiguous, but agreement with acidity peaks in ice cores (Svensson et al. 2013) suggests that our REE events tracks eruption history over the interval discussed here. Our δ<sup>18</sup>O, δ<sup>13</sup>C, and Sr records suggest repeated EASM weakening and regional-scale rainfall reduction in response to volcanic events indicated by REE peaks. Comparison of the REE and Sr profiles further suggests that drying was initiated or exacerbated by these eruptions.</p><p>Our new multi-proxy record supports the hypothesis of repeated tropical eruptions that led to several significant weakening episodes of the EASM. The current data do not answer the question whether the YTT initiated GS20 but support the notion of multi-decadal impacts on regional circulation and rainfall across East Asia.</p><p> </p><p><strong>References: </strong></p><p>Ambrose S. (2003) Population bottleneck, in: Robinson, R. (Ed.), Genetics, volume 3. Macmillan Reference, New York, 167-171</p><p>Ge Y. et al. (2020) Understanding the overestimated impact of the Toba volcanic super-eruption on global environments and ancient hominins. Quat Int. 559, 24-33</p><p>Petraglia M. et al. (2007) Middle Paleolithic Assemblages from the Indian Subcontinent Before and After the Toba Super-Eruption. Science 317, 114-116</p><p>Polyak V. et al. (2017) Rapid speleothem δ<sup>13</sup>C change in southwestern North America coincident with Greenland stadial 20 and the Toba (Indonesia) supereruption. Geology 45, 843-846</p><p>Svensson A. et al. (2013) Direct linking of Greenland and Antarctic ice cores at the Toba eruption (74 ka BP): Climate of the Past 9, 749-766</p>

Population genomic evidence that human and animal infections in Africa come from the same populations of Dracunculus medinensis

Background Guinea worm–Dracunculus medinensis–was historically one of the major parasites of humans and has been known since antiquity. Now, Guinea worm is on the brink of eradication, as efforts to interrupt transmission have reduced the annual burden of disease from millions of infections per year in the 1980s to only 54 human cases reported globally in 2019. Despite the enormous success of eradication efforts to date, one complication has arisen. Over the last few years, hundreds of dogs have been found infected with this previously apparently anthroponotic parasite, almost all in Chad. Moreover, the relative numbers of infections in humans and dogs suggests that dogs are currently the principal reservoir on infection and key to maintaining transmission in that country. Principal findings In an effort to shed light on this peculiar epidemiology of Guinea worm in Chad, we have sequenced and compared the genomes of worms from dog, human and other animal infections. Confirming previous work with other molecular markers, we show that all of these worms are D. medinensis, and that the same population of worms are causing both infections, can confirm the suspected transmission between host species and detect signs of a population bottleneck due to the eradication efforts. The diversity of worms in Chad appears to exclude the possibility that there were no, or very few, worms present in the country during a 10-year absence of reported cases. Conclusions This work reinforces the importance of adequate surveillance of both human and dog populations in the Guinea worm eradication campaign and suggests that control programs aiming to interrupt disease transmission should stay aware of the possible emergence of unusual epidemiology as pathogens approach elimination.

Genetic Markers of Adaptation of Plasmodium falciparum to Transmission by American Vectors Identified in the Genomes of Parasites from Haiti and South America

ABSTRACT The malaria parasite, Plasmodium falciparum, was introduced into Hispaniola and other regions of the Americas through the slave trade spanning the 16th through the 19th centuries. During this period, more than 12 million Africans were brought across the Atlantic to the Caribbean and other regions of the Americas. Since malaria is holoendemic in West Africa, a substantial percentage of these individuals carried the parasite. St. Domingue on Hispaniola, now modern-day Haiti, was a major port of disembarkation, and malaria is still actively transmitted there. We undertook a detailed study of the phylogenetics of the Haitian parasites and those from Colombia and Peru utilizing whole-genome sequencing. Principal-component and phylogenetic analyses, based upon single nucleotide polymorphisms (SNPs) in protein coding regions, indicate that, despite the potential for millions of introductions from Africa, the Haitian parasites share an ancestral relationship within a well-supported monophyletic clade with parasites from South America, while belonging to a distinct lineage. This result, in stark contrast to the historical record of parasite introductions, is best explained by a severe population bottleneck experienced by the parasites introduced into the Americas. Here, evidence is presented for targeted selection of rare African alleles in genes which are expressed in the mosquito stages of the parasite’s life cycle. These genetic markers support the hypothesis that the severe population bottleneck was caused by the required adaptation of the parasite to transmission by new definitive hosts among the Anopheles (Nyssorhynchus) spp. found in the Caribbean and South America. IMPORTANCE Historical data suggest that millions of P. falciparum parasite lineages were introduced into the Americas during the trans-Atlantic slave trade, which would suggest a paraphyletic origin of the extant isolates in the Western Hemisphere. Our analyses of whole-genome variants show that the American parasites belong to a well-supported monophyletic clade. We hypothesize that the required adaptation to American vectors created a severe bottleneck, reducing the effective introduction to a few lineages. In support of this hypothesis, we discovered genes expressed in the mosquito stages of the life cycle that have alleles with multiple, high-frequency or fixed, nonsynonymous mutations in the American populations which are rarely found in African isolates. These alleles appear to be in gene products critical for transmission through the anopheline vector. Thus, these results may inform efforts to develop novel transmission-blocking vaccines by identifying parasite proteins functionally interacting with the vector that are important for successful transmission. Further, to the best of our knowledge, these are the first whole-genome data available from Haitian P. falciparum isolates. Defining the genome of these parasites provides genetic markers useful for mapping parasite populations and monitoring parasite movements/introductions.

Inferring Transmission Bottleneck Size from Viral Sequence Data Using a Novel Haplotype Reconstruction Method

ABSTRACT The transmission bottleneck is defined as the number of viral particles that transmit from one host to establish an infection in another. Genome sequence data have been used to evaluate the size of the transmission bottleneck between humans infected with the influenza virus; however, the methods used to make these estimates have some limitations. Specifically, viral allele frequencies, which form the basis of many calculations, may not fully capture a process which involves the transmission of entire viral genomes. Here, we set out a novel approach for inferring viral transmission bottlenecks; our method combines an algorithm for haplotype reconstruction with maximum likelihood methods for bottleneck inference. This approach allows for rapid calculation and performs well when applied to data from simulated transmission events; errors in the haplotype reconstruction step did not adversely affect inferences of the population bottleneck. Applied to data from a previous household transmission study of influenza A infection, we confirm the result that the majority of transmission events involve a small number of viruses, albeit with slightly looser bottlenecks being inferred, with between 1 and 13 particles transmitted in the majority of cases. While influenza A transmission involves a tight population bottleneck, the bottleneck is not so tight as to universally prevent the transmission of within-host viral diversity. IMPORTANCE Viral populations undergo a repeated cycle of within-host growth followed by transmission. Viral evolution is affected by each stage of this cycle. The number of viral particles transmitted from one host to another, known as the transmission bottleneck, is an important factor in determining how the evolutionary dynamics of the population play out, restricting the extent to which the evolved diversity of the population can be passed from one host to another. Previous study of viral sequence data has suggested that the transmission bottleneck size for influenza A transmission between human hosts is small. Reevaluating these data using a novel and improved method, we largely confirm this result, albeit that we infer a slightly higher bottleneck size in some cases, of between 1 and 13 virions. While a tight bottleneck operates in human influenza transmission, it is not extreme in nature; some diversity can be meaningfully retained between hosts.

Testing the Effect of the Toba Volcanic Eruption on Population Sizes in Worldwide Mammal Species

The volcanic eruption of Toba in northern Sumatra at 71 kyBP (±5 kyBP) emitted sulfur gas and deposited thick layers of dust throughout the surrounding region. It is thought to have had a significant and dramatic cooling impact on the paleoclimate worldwide. Ambrose [1] conjectured this to be the cause of the contemporaneous (50-100 kyBP) population bottleneck observed in humans. We hypothesize that a volcanic winter of sufficient magnitude to cause a population bottleneck in humans would similarly affect other mammals. To test this hypothesis, we estimated pairwise mismatch distributions using mtDNA control region sequences of 28 mammal species archived on NCBI to assess whether each species underwent a population bottleneck. For any species fitting the sudden expansion model, we estimated the timing of the bottleneck and compared it to the date range of the Toba eruption. Only 3 of the 28 species show evidence of rapid population expansion overlapping in time with the Toba eruption. Therefore, the hypothesis that the volcanic winter triggered by the Toba eruption caused a significant bottleneck impacting mammal species worldwide is not supported by mitochondrial evidence. Our results question the hypothesis that the Toba eruption contributed to the bottleneck observed in humans at this time.

Severe population bottleneck and cranial morphology change in the Mednyi Island subspecies of Arctic fox Vulpes lagopus (Carnivora: Canidae)

Arctic foxes, Vulpes lagopus living on Mednyi Island suffered a drastic decline in population size in the late 1970s due to an outbreak of mange epizootic. This dramatic fall in numbers rendered the subspecies endangered, and the concomitant loss of variability resulted in a population bottleneck. Here, we investigate whether differences in cranial morphology between Mednyi Island Arctic foxes and Bering Island Arctic foxes could be attributed to the severe population bottleneck suffered by the Mednyi population in the 1970s. We used morphometric traits as proxies for genetic data to provide estimates of FST. Results show higher FST estimates for the Mednyi population than for the Bering population, which we interpret as a bottleneck signature. FST results also indicate a pattern of divergence between the two populations consistent with random genetic drift. Bottleneck detection is critical for the interpretation of the demographic history of the endangered Mednyi Island Arctic fox, with consequences for conservation management.