The endangered White Sands pupfish (Cyprinodon tularosa) genome reveals low diversity and heterogenous patterns of differentiation

Black, Andrew N.; Willoughby, Janna R.; Brüniche‐Olsen, Anna; Pierce, Brian L.; DeWoody, J. Andrew

doi:10.1111/1755-0998.13447

Cited by 4 publications

(6 citation statements)

References 80 publications

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“…2 A ). Consistent with Black et al ( 22 ), individual heterozygosity among all 45 samples was very low and varied by a factor of three across sites, ranging from 0.00046 (LR) to 0.00149 (MS). Significant genome-wide differences in heterozygosity were observed across pairwise population comparisons (Wilcoxon signed rank test, W = 0 to 42, P -values < 0.003).…”

Section: Divergence Timessupporting

confidence: 86%

“…Whole-genome library preparation and sequencing were conducted on individually barcoded samples (n = 15 from each population) and on three pools of samples (n = 30 from each population). Quality controlled reads were aligned to the C. tularosa reference genome ( 22 ) with bwa ( 58 ) and were processed using Poolparty ( 59 ) and Angsd ( 60 ), which were also used to estimate individual heterozygosity and pairwise differentiation. Population structure was evaluated using PCAngsd ( 61 ), NGSadmix ( 62 ), and runs of homozygosity were identified using bcftools ( 63 ).…”

Section: Methodsmentioning

confidence: 99%

“…We note that all three populations had very low levels of genomic diversity, as evidenced by the identification of only ~200 to 400k genomic polymorphisms and overall heterozygosity levels ~0.009 (see also ref. 22 ). To our knowledge, there is no established safeguard against the extirpation of the MS population.…”

Section: Divergence Timesmentioning

confidence: 99%

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Rapid vertebrate speciation via isolation, bottlenecks, and drift

Black,

Heenkenda,

Mathur

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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Speciation is often driven by selective processes like those associated with viability, mate choice, or local adaptation, and “speciation genes” have been identified in many eukaryotic lineages. In contrast, neutral processes are rarely considered as the primary drivers of speciation, especially over short evolutionary timeframes. Here, we describe a rapid vertebrate speciation event driven primarily by genetic drift. The White Sands pupfish ( Cyprinodon tularosa ) is endemic to New Mexico’s Tularosa Basin where the species is currently managed as two Evolutionarily significant units (ESUs) and is of international conservation concern (Endangered). Whole-genome resequencing data from each ESU showed remarkably high and uniform levels of differentiation across the entire genome (global F ST ≈ 0.40). Despite inhabiting ecologically dissimilar springs and streams, our whole-genome analysis revealed no discrete islands of divergence indicative of strong selection, even when we focused on an array of candidate genes. Demographic modeling of the joint allele frequency spectrum indicates the two ESUs split only ~4 to 5 kya and that both ESUs have undergone major bottlenecks within the last 2.5 millennia. Our results indicate the genome-wide disparities between the two ESUs are not driven by divergent selection but by neutral drift due to small population sizes, geographic isolation, and repeated bottlenecks. While rapid speciation is often driven by natural or sexual selection, here we show that isolation and drift have led to speciation within a few thousand generations. We discuss these evolutionary insights in light of the conservation management challenges they pose.

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Section: Divergence Timessupporting

confidence: 86%

Section: Methodsmentioning

confidence: 99%

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Rapid vertebrate speciation via isolation, bottlenecks, and drift

Black,

Heenkenda,

Mathur

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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“…variegatus mitogenomes, as was also observed by Lema, Wilson, et al (2016). Recent unpublished nuclear DNA analyses suggest possible genetic introgression of C. variegatus into C. tularosa (Black et al 2021), which may explain relationships of those taxa in Figure 1.…”

supporting

confidence: 68%

Complete mitochondrial genome of the Salt Creek pupfish, Cyprinodon salinus salinus: characterization and identification of single nucleotide polymorphisms (SNPs)

Core

Cleveland

Lema

2021

Mitochondrial DNA Part B

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The Salt Creek pupfish, Cyprinodon salinus salinus Miller, 1943 is endemic to Death Valley, California, USA, and resides as a single population within one of the most extreme inland aquatic environments capable of supporting fish. Here we report the sequencing of complete 16,499 base pair (bp) mitochondrion genomes from four C. salinus salinus individuals. The mitochondrial genome of C. salinus salinus comprises 13 protein-coding regions, 12S and 16S rRNAs, 22 tRNAs, and an 832 bp D-loop region. The first reported single nucleotide polymorphisms (SNPs) were identified within the mtDNA of C. salinus salinus, with the four mitogenomes exhibiting only 0.0485% nucleotide sequence divergence indicative of low intraspecific variation. These complete mitogenomes will facilitate future genetic analyses of intraspecific diversity between the two described subspecies of C. salinus as well as other Cyprinodon pupfishes in southwestern North America.

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“…They reinforce Mossop et al’s [ 35 ] conclusion that ephemeral waters represent important dispersal routes in arid ecosystems. Such connections, however fleeting, seem to help freshwater fishes in isolated waters to overcome the small population sizes and low genetic diversity [ 96 – 99 ] that could otherwise promote a drift towards imperilment or extinction.…”

Section: Discussionmentioning

confidence: 99%

Genetic approaches reveal a healthy population and an unexpectedly recent origin for an isolated desert spring fish

Sidlauskas,

Mathur,

Aydoğan

et al. 2024

BMC Ecol Evo

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Foskett Spring in Oregon’s desert harbors a historically threatened population of Western Speckled Dace (Rhinichthys klamathensis). Though recently delisted, the dace’s recruitment depends upon regular removal of encroaching vegetation. Previous studies assumed that Foskett Dace separated from others in the Warner Valley about 10,000 years ago, thereby framing an enigma about the population’s surprising ability to persist for so long in a tiny habitat easily overrun by plants. To investigate that persistence and the effectiveness of interventions to augment population size, we assessed genetic diversity among daces inhabiting Foskett Spring, a refuge at Dace Spring, and three nearby streams. Analysis revealed a robust effective population size (Ne) of nearly 5000 within Foskett Spring, though Ne in the Dace Spring refuge is just 10% of that value. Heterozygosity is slightly lower than expected based on random mating at all five sites, indicating mild inbreeding, but not at a level of concern. These results confirm the genetic health of Foskett Dace. Unexpectedly, genetic differentiation reveals closer similarity between Foskett Dace and a newly discovered population from Nevada’s Coleman Creek than between Foskett Dace and dace elsewhere in Oregon. Demographic modeling inferred Coleman Creek as the ancestral source of Foskett Dace fewer than 1000 years ago, much more recently than previously suspected and possibly coincident with the arrival of large herbivores whose grazing may have maintained open water suitable for reproduction. These results solve the enigma of persistence by greatly shortening the duration over which Foskett Dace have inhabited their isolated spring.

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The endangered White Sands pupfish (Cyprinodon tularosa) genome reveals low diversity and heterogenous patterns of differentiation

Cited by 4 publications

References 80 publications

Rapid vertebrate speciation via isolation, bottlenecks, and drift

Rapid vertebrate speciation via isolation, bottlenecks, and drift

Complete mitochondrial genome of the Salt Creek pupfish, Cyprinodon salinus salinus: characterization and identification of single nucleotide polymorphisms (SNPs)

Genetic approaches reveal a healthy population and an unexpectedly recent origin for an isolated desert spring fish

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