Natural selection shaped the rise and fall of passenger pigeon genomic diversity

Murray, Gemma G. R.; Soares, André Elias Rodrigues; Novak, Ben J.; Schaefer, Nathan K.; Cahill, James A.; Baker, Allan J.; Demboski, John R.; Doll, Andrew C.; Fonseca, Rute R. da; Fulton, Tara L.; Gilbert, Martin; Heintzman, Peter D.; Letts, Brandon; McInstosh, George; O’Connell, Brendan; Peck, Mark; Pipes, Marie-Lorraine; Rice, Edward S.; Santos, Kathryn M.; Sohrweide, A. Gregory; Vohr, Samuel H.; Corbett-Detig, Russell; Green, Edward; Shapiro, Beth

doi:10.1101/154294

Cited by 27 publications

(37 citation statements)

References 32 publications

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“…6), as was also observed in the Passenger Pigeon genome (Murray et al. ). The ratio of autosomal to Z‐linked π ranges from 0.44 to 0.58 across species (Table )—lower than the 0.75 ratio predicted by population size effects alone (Table ).…”

Section: Resultssupporting

confidence: 71%

“…In the passenger and band‐tailed pigeons (Ectopistes migratorius and Patagioenas fasciata), regions of elevated nucleotide diversity (π) occur in parts of the genome with high recombination rates, and the strength of this relationship appears to vary with effective population size (Murray et al. ). Because selection should be more effective in larger populations and will remove diversity from larger chunks of the chromosome in regions with low recombination, these results suggest that linked selection could explain much of the variation in diversity across the genome of these species.…”

Section: Natural History Of Northern Selasphorus Hummingbirdsmentioning

confidence: 99%

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Evidence of linked selection on the Z chromosome of hybridizing hummingbirds*

Battey

2020

Evolution

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Levels of genetic differentiation vary widely along the genomes of recently diverged species. What processes cause this variation?Here, I analyze geographic population structure and genome-wide patterns of variation in the Rufous, Allen's, and Calliope Hummingbirds (Selasphorus rufus/Selasphorus sasin/Selasphorus calliope) and assess evidence that linked selection on theZ chromosome drives patterns of genetic differentiation in a pair of hybridizing species. Demographic models, introgression tests, and genotype clustering analyses support a reticulate evolutionary history consistent with divergence during the late Pleistocene followed by gene flow across migrant Rufous and Allen's Hummingbirds during the Holocene. Relative genetic differentiation (F st ) is elevated, and within-population diversity (π) is depressed on the Z chromosome in all interspecific comparisons. The ratio of Z to autosomal within-population diversity is much lower than that expected from population size effects alone, and Tajima's D is depressed on the Z chromosome in S. rufus and S. calliope. These results suggest that conserved structural features of the genome play a prominent role in shaping genetic differentiation through the early stages of speciation in northern Selasphorus hummingbirds, and that the Z chromosome is a likely site of genes underlying behavioral and morphological variation in the group.

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Section: Resultssupporting

confidence: 71%

Section: Natural History Of Northern Selasphorus Hummingbirdsmentioning

confidence: 99%

Evidence of linked selection on the Z chromosome of hybridizing hummingbirds*

Battey

2020

Evolution

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“…This approach was used by Murray et al. (2017) in their analysis of DNA from museum samples of the once abundant but now extinct passenger pigeon ( Ectopistes migratorius ). Hung et al.…”

Section: Detecting Purifying Selectionmentioning

confidence: 99%

Inference of natural selection from ancient DNA

Dehasque

Ávila‐Arcos²,

Díez-del-Molino

et al. 2020

Evolution Letters

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Evolutionary processes, including selection, can be indirectly inferred based on patterns of genomic variation among contemporary populations or species. However, this often requires unrealistic assumptions of ancestral demography and selective regimes.Sequencing ancient DNA from temporally spaced samples can inform about past selection processes, as time series data allow direct quantification of population parameters collected before, during, and after genetic changes driven by selection. In this 9 4Comment and Opinion, we advocate for the inclusion of temporal sampling and the generation of paleogenomic datasets in evolutionary biology, and highlight some of the recent advances that have yet to be broadly applied by evolutionary biologists.In doing so, we consider the expected signatures of balancing, purifying, and positive selection in time series data, and detail how this can advance our understanding of the chronology and tempo of genomic change driven by selection. However, we also recognize the limitations of such data, which can suffer from postmortem damage, fragmentation, low coverage, and typically low sample size. We therefore highlight the many assumptions and considerations associated with analyzing paleogenomic data and the assumptions associated with analytical methods. K E Y W O R D S : Adaptation, ancient DNA, natural selection, paleogenomics, time series. Impact SummaryThe search for signatures of natural selection on the genome is still most commonly based on screening modern genomes for regions of reduced diversity or increased differentiation between populations. This framework is essentially a snapshot in time of a process that may have played out over many millennia, during which changes in population size, ecology and gene flow between populations may have played a role in determining genetic variation. Here, we outline how utilising ancient DNA (aDNA) techniques to sequence time series of genomes spanning changes in natural selection can provide a more nuanced understanding of how natural selection has impacted genomic variation in present-day populations. In particular, we argue that the advent of paleo-population genomics, in which datasets of multiple individuals spanning millennia have been sequenced, offers unprecedented opportunity to estimate changes in allele frequencies through time. We outline considerations and the types of data that would be needed for the inference of positive selection on traits associated with single and many genes (polygenic), genome-wide negative (background) selection, and balancing selection. However, we recognise that there are currently few datasets existing that are suitable for these types of investigation. There is thus a bias towards study species that have undergone strong selection over relatively recent timescales that are within the scope of aDNA, such as has occurred in domesticated species. We also detail a number of caveats associated with working with aDNA data, which is by its nature comprised of short, degraded DNA fragments, typicall...

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“…Some bird species have exceedingly large flocks accounting for huge total numbers of individuals such as the extinct passenger pigeon Ectopistes migratorius (several billion individuals), brambling Fringilla montifringilla (418 million), red‐billed quelea Quelea quelea (217 million), and European starling (133 million). The passenger pigeon has been considered to represent a species apart due to its exceedingly large fluctuations in numbers and the crucial role of sociality for the maintenance of viability (Hung et al, ; Murray et al, ). We doubt that any other species resembles the passenger pigeon in its role of sociality for the maintenance of huge flocks.…”

Section: Discussionmentioning

confidence: 99%

The ecological significance of extremely large flocks of birds

Møller

Laursen

2019

Ecology and Evolution

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Population size is generally limited by resource availability during and outside the breeding season. Therefore, maximum size of flocks may provide important information on population regulation and the influence of diet and trophic level on maximal degree of sociality. We hypothesized that (a) flock size should increase with nutrient availability; (b) flock size should decrease with latitude because productivity is higher at lower latitude; (c) aquatic habitats should have larger flocks than terrestrial habitats because the former are less accessible; (d) smaller species should have larger flocks because they require overall less food; (e) human‐impacted species that live in perturbed habitats should have smaller flocks than other species; (f) flock size should decrease with increasing trophic level because there is a reduction in biomass due to conversion at each trophic level; and (g) flocks of species depending on ancestral landscapes should have decreased in size in recent years due to human impact (e.g., land‐use). We obtained 1564 observations of flocks that exceeded 100,000 individuals in order to test the predictions listed above. Most effect sizes were small to medium accounting for 1%–9% of the variance, while large effects accounting for 25% or more were only found for total nitrogen used per km2 and area used for agriculture. Changes in large bird flocks were caused by habitat degradation and persecution, and temporal decline in size of large flocks revealed changes in nutrient use, reductions in nutrient cycling, and changes in flock size linked to trophic level.

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Natural selection shaped the rise and fall of passenger pigeon genomic diversity

Cited by 27 publications

References 32 publications

Evidence of linked selection on the Z chromosome of hybridizing hummingbirds*

Evidence of linked selection on the Z chromosome of hybridizing hummingbirds*

Inference of natural selection from ancient DNA

The ecological significance of extremely large flocks of birds

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