Evidence for Late Pleistocene origin of Astyanax mexicanus cavefish

AbstractBackgroundCavefish populations belonging to the Mexican tetra species Astyanax mexicanus are outstanding models to study the tempo and mode of adaptation to a radical environmental change. They share similar phenotypic changes such as blindness and depigmentation resulting from independent and convergent evolution. As such they allow examining whether their evolution involved the fixation of preexisting standing genetic variations and/or de novo mutations. Cavefish populations are currently assigned to two main groups, the so-called "old" and "new" lineages, which would have populated several caves independently and at different times. However, we do not have yet accurate estimations of the time frames of evolution of these populations.ResultsFirst, we reanalyzed the geographic distribution of mitochondrial and nuclear DNA polymorphisms and we found that these data do not support the existence of two cavefish lineages, neither the ancient origin of the “old” lineage. Using IMa2, a program based on a method that does not assume that populations are at mutation/migration/drift equilibrium and thus allows dating population divergence in addition to demographic parameters, we found that microsatellite polymorphism strongly supports a very recent origin of cave populations (i.e. less than 20,000 years). Second, we identified a large number of single-nucleotide polymorphisms (SNPs) in transcript sequences of pools of embryos (Pool-seq) belonging to the “old” Pachón cave population and a surface population from Texas. Pachón cave population has accumulated more neutral substitutions than the surface population and we showed that it could be another signature of its recent origin. Based on summary statistics that can be computed with this SNP data set together with simulations of evolution of SNP polymorphisms in two recently isolated populations, we looked for sets of demographic parameters that allow the computation of summary statistics with simulated populations that are similar to the ones with the sampled populations. In most simulations for which we could find a good fit between the summary statistics of observed and simulated data, the best fit occurred when the divergence between simulated populations was less than 30,000 years.ConclusionsAlthough it is often assumed that some cave populations such as Pachón cavefish have a very ancient origin, within the range of the late Miocene to the middle Pleistocene, a recent origin of these populations is strongly supported by our analyses of two independent sets of nuclear DNA polymorphism using two very different methods of analysis. Moreover, the observation of two divergent haplogroups of mitochondrial and nuclear genes with different geographic distributions support a recent admixture of two divergent surface populations before the isolation of cave populations. If cave populations are indeed only several thousand years old, many phenotypic changes observed in cavefish would thus have mainly involved the fixation of genetic variants present in surface fish populations and within a very short period of time.

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Evidence for rapid phenotypic and behavioural shifts in a recently established cavefish population

Biological Journal of the Linnean Society ◽

10.1093/biolinnean/blz162 ◽

2019 ◽

Author(s):

Suzanne E McGaugh ◽

Sam Weaver ◽

Erin N Gilbertson ◽

Brianna Garrett ◽

Melissa L Rudeen ◽

...

Keyword(s):

Extreme Environments ◽

Time Frame ◽

South Texas ◽

Astyanax Mexicanus ◽

North East ◽

Surface Population ◽

Cave Population ◽

Cave Environment ◽

Central Texas ◽

Recent Origin

Abstract Cave colonization offers a natural laboratory to study an extreme environmental shift, and diverse cave species from around the world often have converged on robust morphological, physiological and behavioural traits. The Mexican tetra (Astyanax mexicanus) has repeatedly colonized caves in the Sierra de El Abra and Sierra de Guatemala regions of north-east Mexico ~0.20–1 Mya, indicating an ability to adapt to the cave environment. The time frame for the evolution of these traits in any cave animal, however, is poorly understood. Astyanax mexicanus from the Río Grande in South Texas were brought to Central Texas beginning in the early 1900s and colonized underground environments. Here, we investigate whether phenotypic and behavioural differences have occurred rapidly between a surface population and a geographically proximate cave population, probably of recent origin. Fish from the cave and surface populations differ significantly in morphological traits, including coloration, lateral line expansion and dorsal fin placement. Striking behavioural shifts in aggression, feeding and wall-following have also occurred. Together, our results suggest that morphological and behavioural changes accompanying cave colonization can be established rapidly, and this system offers an exciting and unique opportunity for isolating the genetic and environmental contributions to colonization of extreme environments.

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Evidence for rapid phenotypic and behavioral change in a recently established cavefish population

10.1101/651406 ◽

2019 ◽

Author(s):

Suzanne E. McGaugh ◽

Sam Weaver ◽

Erin N. Gilbertson ◽

Brianna Garrett ◽

Melissa L. Rudeen ◽

...

Keyword(s):

Behavioral Change ◽

Extreme Environments ◽

Behavioral Differences ◽

Astyanax Mexicanus ◽

Eye Size ◽

Exciting Opportunity ◽

Surface Population ◽

Cave Population ◽

Future Work ◽

Rapid Environmental Change

AbstractSubstantial morphological and behavioral shifts often accompany rapid environmental change, yet, little is known about the early stages of cave colonization. Relative to surface streams, caves are extreme environments with perpetual darkness and low nutrient availability. The Mexican tetra (Astyanax mexicanus), has repeatedly colonized caves throughout Mexico, suggesting an ability to adapt to these conditions. Here, we survey for phenotypic and behavioral differences between a surface population and a cave population of A. mexicanus that has recently colonized Honey Creek Cave, Comal County, Texas, likely within the last century. We found that fish from Honey Creek Cave and fish from Honey Creek surface populations differ significantly in morphological traits including length, coloration, body condition, eye size, and dorsal fin placement. Cavefish also exhibit an increased number of superficial neuromasts relative to surface fish. Behaviorally, cavefish consume fewer worms when trials are performed in both lighted and darkened conditions. Cavefish are more aggressive than surface fish and exhibit fewer behaviors associated with stress. Further in contrast to surface fish, cavefish prefer the edges to the center of an arena and are qualitatively more likely to investigate a novel object placed in the tank. While cavefish and surface fish were wild-caught and developmental environment likely play a role in shaping these differences, our work demonstrates morphological and behavioral shifts for Texas cavefish and offers an exciting opportunity for future work to explore the genetic and environmental contributions to early cave colonization.

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Matching loci surveyed to questions asked in phylogeography

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.2340 ◽

2016 ◽

Vol 283 (1826) ◽

pp. 20152340 ◽

Cited By ~ 19

Author(s):

Chih-Ming Hung ◽

Sergei V. Drovetski ◽

Robert M. Zink

Keyword(s):

Population Diversity ◽

Single Locus ◽

Population Divergence ◽

Summary Statistics ◽

Recent Past ◽

Size Change ◽

The Caucasus ◽

Nuclear Loci ◽

The Difference ◽

Coalescent Time

Although mitochondrial DNA (mtDNA) has long been used for assessing genetic variation within and between populations, its workhorse role in phylogeography has been criticized owing to its single-locus nature. The only choice for testing mtDNA results is to survey nuclear loci, which brings into contrast the difference in locus effective size and coalescence times. Thus, it remains unclear how erroneous mtDNA-based estimates of species history might be, especially for evolutionary events in the recent past. To test the robustness of mtDNA and nuclear sequences in phylogeography, we provide one of the largest paired comparisons of summary statistics and demographic parameters estimated from mitochondrial, five Z-linked and 10 autosomal genes of 30 avian species co-distributed in the Caucasus and Europe. The results suggest that mtDNA is robust in estimating inter-population divergence but not in intra-population diversity, which is sensitive to population size change. Here, we provide empirical evidence showing that mtDNA was more likely to detect population divergence than any other single locus owing to its smaller N e and thus faster coalescent time. Therefore, at least in birds, numerous studies that have based their inferences of phylogeographic patterns solely on mtDNA should not be readily dismissed.

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Pliocene Origin, Ice Ages and Postglacial Population Expansion Have Influenced a Panmictic Phylogeography of the European Bee-Eater Merops apiaster

Diversity ◽

10.3390/d11010012 ◽

2019 ◽

Vol 11 (1) ◽

pp. 12 ◽

Cited By ~ 4

Author(s):

Carina Carneiro de Melo Moura ◽

Hans-Valentin Bastian ◽

Anita Bastian ◽

Erjia Wang ◽

Xiaojuan Wang ◽

...

Keyword(s):

Genetic Differentiation ◽

Nuclear Dna ◽

Bird Species ◽

Population Expansion ◽

Genetic Connectivity ◽

Middle Pleistocene ◽

Ice Ages ◽

Breeding Sites ◽

Late Tertiary ◽

Merops Apiaster

Oscillations of periods with low and high temperatures during the Quaternary in the northern hemisphere have influenced the genetic composition of birds of the Palearctic. During the last glaciation, ending about 12,000 years ago, a wide area of the northern Palearctic was under lasting ice and, consequently, breeding sites for most bird species were not available. At the same time, a high diversity of habitats was accessible in the subtropical and tropical zones providing breeding grounds and refugia for birds. As a result of long-term climatic oscillations, the migration systems of birds developed. When populations of birds concentrated in refugia during ice ages, genetic differentiation and gene flow between populations from distinct areas was favored. In the present study, we explored the current genetic status of populations of the migratory European bee-eater. We included samples from the entire Palearctic-African distribution range and analyzed them via mitochondrial and nuclear DNA markers. DNA data indicated high genetic connectivity and panmixia between populations from Europe, Asia and Africa. Negative outcomes of Fu’s Fs and Tajima’s D tests point to recent expansion events of the European bee-eater. Speciation of Merops apiaster started during the Pliocene around three million years ago (Mya), with the establishment of haplotype lineages dated to the Middle Pleistocene period circa 0.7 Mya. M. apiaster, which breed in Southern Africa are not distinguished from their European counterparts, indicating a recent separation event. The diversification process of the European bee-eater was influenced by climatic variation during the late Tertiary and Quaternary. Bee-eaters must have repeatedly retracted to refugia in the Mediterranean and subtropical Africa and Asia during ice ages and expanded northwards during warm periods. These processes favored genetic differentiation and repeated lineage mixings, leading to a genetic panmixia, which we still observe today.

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Contrasts between the phylogeographic patterns of chloroplast and nuclear DNA highlight a role for pollen-mediated gene flow in preventing population divergence in an East Asian temperate tree

Molecular Phylogenetics and Evolution ◽

10.1016/j.ympev.2014.08.024 ◽

2014 ◽

Vol 81 ◽

pp. 37-48 ◽

Cited By ~ 37

Author(s):

Wei-Ning Bai ◽

Wen-Ting Wang ◽

Da-Yong Zhang

Keyword(s):

Gene Flow ◽

Nuclear Dna ◽

East Asian ◽

Population Divergence

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Contrasted gene decay in subterranean vertebrates: insights from cavefishes and fossorial mammals

10.1101/2020.03.05.978213 ◽

2020 ◽

Cited By ~ 3

Author(s):

Maxime Policarpo ◽

Julien Fumey ◽

Philippe Lafargeas ◽

Delphine Naquin ◽

Claude Thermes ◽

...

Keyword(s):

Evolutionary Process ◽

Sharp Contrast ◽

Functional Constraints ◽

Loss Of Function ◽

Astyanax Mexicanus ◽

Gene Sets ◽

Cave Population ◽

Cave Ecosystems ◽

Genome Ploidy ◽

Gene Decay

AbstractEvolution sometimes proceeds by loss, especially when structures and genes become dispensable after an environmental shift relaxing functional constraints. Gene decay can serve as a read-out of this evolutionary process. Animals living in the dark are outstanding models, in particular cavefishes as hundreds of species evolved independently during very different periods of time in absence of light. Here, we sought to understand some general principals on the extent and tempo of decay of several gene sets in cavefishes. The analysis of the genomes of two Cuban species belonging to the genus Lucifuga provides evidence for the most massive loss of eye genes reported so far in cavefishes. Comparisons with a recently-evolved cave population of Astyanax mexicanus and three species belonging to the tetraploid Chinese genus Sinocyclocheilus revealed the combined effects of the level of eye regression, time and genome ploidy on the number of eye pseudogenes. In sharp contrast, most circadian clock and pigmentation genes appeared under strong selection. In cavefishes for which complete genomes are available, the limited extent of eye gene decay and the very small number of loss of function (LoF) mutations per pseudogene suggest that eye degeneration is never very ancient, ranging from early to late Pleistocene. This is in sharp contrast with the identification of several eye pseudogenes carrying many LoF mutations in ancient fossorial mammals. Our analyses support the hypothesis that blind fishes cannot thrive more than a few millions of years in cave ecosystems.

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Untargeted Metabolomics of the Cavefish Astyanax mexicanus Reveals the Basis of Metabolic Strategies in Adaptation to Extreme Conditions

10.1101/2020.10.27.358077 ◽

2020 ◽

Author(s):

J Kyle Medley ◽

Jenna Persons ◽

Robert Peuß ◽

Luke Olsen ◽

Shaolei Xiong ◽

...

Keyword(s):

Behavioral Changes ◽

Protein Glycation ◽

Untargeted Metabolomics ◽

Short Term ◽

Astyanax Mexicanus ◽

Surface Population ◽

Shiny App ◽

Metabolomics Study ◽

Metabolic Strategies

The Mexican tetra, Astyanax mexicanus, has undergone remarkable physiological and behavioral changes in order to colonize a number of subterranean caves in the Sierra de El Abra region of Mexico. A hallmark of cave-adapted populations is enhanced survival under low-nutrient conditions coupled with hyperglycemia, increased body fat, and insulin resistance, but cavefish appear to avoid the progression of the respective pathologies associated with these conditions and do not exhibit reduced longevity. The metabolic strategies underlying these adaptations are not fully understood. Here, we provide an untargeted metabolomics study of longand short-term fasting in two A. mexicanus cave populations and one surface population. We find that, although cavefish share many similarities with metabolic syndrome normally associated with the human state of obesity, important differences emerge, including cholesterol esters, urate, intermediates of protein glycation, metabolites associated with hypoxia and longevity, and unexpectedly elevated levels of ascorbate (vitamin C). This work highlights the fact that certain metabolic features associated with human pathologies are not intrinsically harmful in all organisms, and suggests promising avenues for future investigation into the role of certain metabolites in evolutionary adaptation and health. We provide a transparent pipeline for reproducing our analysis and a Shiny app for other researchers to explore and visualize our dataset.

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A Unique Recent Origin of the Allotetraploid Species Arabidopsis suecica: Evidence from Nuclear DNA Markers

Molecular Biology and Evolution ◽

10.1093/molbev/msk006 ◽

2006 ◽

Vol 23 (6) ◽

pp. 1217-1231 ◽

Cited By ~ 83

Author(s):

Mattias Jakobsson ◽

Jenny Hagenblad ◽

Simon Tavaré ◽

Torbjörn Säll ◽

Christer Halldén ◽

...

Keyword(s):

Dna Markers ◽

Nuclear Dna ◽

Recent Origin ◽

Nuclear Dna Markers ◽

Arabidopsis Suecica ◽

Allotetraploid Species

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Contrasting Gene Decay in Subterranean Vertebrates: Insights from Cavefishes and Fossorial Mammals

Molecular Biology and Evolution ◽

10.1093/molbev/msaa249 ◽

2020 ◽

Cited By ~ 2

Author(s):

Maxime Policarpo ◽

Julien Fumey ◽

Philippe Lafargeas ◽

Delphine Naquin ◽

Claude Thermes ◽

...

Keyword(s):

Specific Gene ◽

Functional Constraints ◽

Limited Extent ◽

Loss Of Function ◽

Astyanax Mexicanus ◽

Cave Population ◽

Opsin Genes ◽

Cave Ecosystems ◽

Genome Ploidy ◽

Gene Decay

Abstract Evolution sometimes proceeds by loss, especially when structures and genes become dispensable after an environmental shift relaxes functional constraints. Subterranean vertebrates are outstanding models to analyze this process, and gene decay can serve as a readout. We sought to understand some general principles on the extent and tempo of the decay of genes involved in vision, circadian clock, and pigmentation in cavefishes. The analysis of the genomes of two Cuban species belonging to the genus Lucifuga provided evidence for the largest loss of eye-specific genes and nonvisual opsin genes reported so far in cavefishes. Comparisons with a recently evolved cave population of Astyanax mexicanus and three species belonging to the Chinese tetraploid genus Sinocyclocheilus revealed the combined effects of the level of eye regression, time, and genome ploidy on eye-specific gene pseudogenization. The limited extent of gene decay in all these cavefishes and the very small number of loss-of-function mutations per pseudogene suggest that their eye degeneration may not be very ancient, ranging from early to late Pleistocene. This is in sharp contrast with the identification of several vision genes carrying many loss-of-function mutations in ancient fossorial mammals, further suggesting that blind fishes cannot thrive more than a few million years in cave ecosystems.

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