Longer or shorter spines: Reciprocal trait evolution in stickleback via triallelic regulatory changes in Stanniocalcin2a

Vertebrates have repeatedly modified skeletal structures to adapt to their environments. The threespine stickleback is an excellent system for studying skeletal modifications, as different wild populations have either increased or decreased the lengths of their prominent dorsal and pelvic spines in different freshwater environments. Here we identify a regulatory locus that has a major morphological effect on the length of stickleback dorsal and pelvic spines, which we term Maser (major spine enhancer). Maser maps in a closely linked supergene complex that controls multiple armor, feeding, and behavioral traits on chromosome IV. Natural alleles in Maser are differentiated between marine and freshwater sticklebacks; however, alleles found among freshwater populations are also differentiated, with distinct alleles found in short- and long-spined freshwater populations. The distinct freshwater alleles either increase or decrease expression of the bone growth inhibitor gene Stanniocalcin2a in developing spines, providing a simple genetic mechanism for either increasing or decreasing spine lengths in natural populations. Genomic surveys suggest many recurrently differentiated loci in sticklebacks are similarly specialized into three or more distinct alleles, providing multiple ancient standing variants in particular genes that may contribute to a range of phenotypes in different environments.

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Should I stay or should I go? The Ectodysplasin locus is associated with behavioural differences in threespine stickleback

Biology Letters ◽

10.1098/rsbl.2009.0416 ◽

2009 ◽

Vol 5 (6) ◽

pp. 788-791 ◽

Cited By ~ 21

Author(s):

Rowan D. H. Barrett ◽

Tim H. Vines ◽

Jason S. Bystriansky ◽

Patricia M. Schulte

Keyword(s):

Positive Selection ◽

Local Adaptation ◽

Morphological Traits ◽

Genetic Basis ◽

Natural Populations ◽

Threespine Stickleback ◽

Adaptive Divergence ◽

Freshwater Habitats ◽

Repeated Evolution ◽

Freshwater Environments

Adaptive divergence may be facilitated if morphological and behavioural traits associated with local adaptation share the same genetic basis. It is therefore important to determine whether genes underlying adaptive morphological traits are associated with variation in behaviour in natural populations. Positive selection on low-armour alleles at the Ectodysplasin ( Eda ) locus in threespine stickleback has led to the repeated evolution of reduced armour, following freshwater colonization by fully armoured marine sticklebacks. This adaptive divergence in armour between marine and freshwater populations would be facilitated if the low allele conferred a behavioural preference for freshwater environments. We experimentally tested whether the low allele is associated with preference for freshwater by measuring the preference of each Eda genotype for freshwater versus saltwater after acclimation to either salinity. We found no association between the Eda low allele and preference for freshwater. Instead, the low allele was significantly associated with a reduced preference for the acclimation environment. This behaviour may facilitate the colonization of freshwater habitats from the sea, but could also hinder local adaptation by promoting migration of low alleles between marine and freshwater environments.

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Genetic analysis of medfly populations in an area of sterile insect technique applications

Journal of Pest Science ◽

10.1007/s10340-021-01337-8 ◽

2021 ◽

Author(s):

Rubén Sancho ◽

Ana Guillem-Amat ◽

Elena López-Errasquín ◽

Lucas Sánchez ◽

Félix Ortego ◽

...

Keyword(s):

Genetic Markers ◽

Sterile Insect Technique ◽

Ceratitis Capitata ◽

Natural Populations ◽

Low Frequency ◽

Fruit Fly ◽

Wild Populations ◽

Genetic Sexing ◽

Environmental Implications ◽

Genetic Sexing Strains

AbstractThe sterile insect technique (SIT) is widely used in integrated pest management programs for the control of the Mediterranean fruit fly (medfly), Ceratitis capitata. The genetic interactions between the released individuals from the genetic sexing strains (GSS), used for SIT applications worldwide, and wild individuals have not been studied. Under the hypothesis that a number of Vienna GSS individuals released to the field might not be completely sterile and may produce viable offspring, we have analyzed medfly Spanish field populations to evaluate the presence of Vienna strain genetic markers. To this goal, we have used contrasted nuclear and mitochondrial genetic markers, and two novel sets of nuclear polymorphisms with the potential to be markers to discriminate between Vienna and wild individuals. Nuclear Vienna markers located on the 5th chromosome of Vienna males have been found in 2.2% (19 from 875) of the Spanish wild medfly females captured at the area where SIT is applied. In addition, a female-inherited mitochondrial Vienna marker has been found in two from the 19 females showing nuclear Vienna markers. The detection of several of these markers in single individuals represents evidence of the introgression of Vienna strain into natural populations. However, alternative explanations as their presence at low frequency in wild populations in the studied areas cannot be fully discarded. The undesired release of non-fully sterile irradiated GSS individuals into the field and their interactions with wild flies, and the potential environmental implications should be taken into account in the application of the SIT.

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Heritability of DNA methylation in threespine stickleback (Gasterosteus aculeatus)

Genetics ◽

10.1093/genetics/iyab001 ◽

2021 ◽

Vol 217 (1) ◽

Author(s):

Juntao Hu ◽

Sara J S Wuitchik ◽

Tegan N Barry ◽

Heather A Jamniczky ◽

Sean M Rogers ◽

...

Keyword(s):

Dna Methylation ◽

Genetic Architecture ◽

Gasterosteus Aculeatus ◽

Additive Genetic Variance ◽

Natural Populations ◽

Threespine Stickleback ◽

Phenotypic Change ◽

Cpg Sites ◽

Cis And Trans ◽

Methylation Variation

Abstract Epigenetic mechanisms underlying phenotypic change are hypothesized to contribute to population persistence and adaptation in the face of environmental change. To date, few studies have explored the heritability of intergenerationally stable methylation levels in natural populations, and little is known about the relative contribution of cis- and trans-regulatory changes to methylation variation. Here, we explore the heritability of DNA methylation, and conduct methylation quantitative trait loci (meQTLs) analysis to investigate the genetic architecture underlying methylation variation between marine and freshwater ecotypes of threespine stickleback (Gasterosteus aculeatus). We quantitatively measured genome-wide DNA methylation in fin tissue using reduced representation bisulfite sequencing of F1 and F2 crosses, and their marine and freshwater source populations. We identified cytosines (CpG sites) that exhibited stable methylation levels across generations. We found that additive genetic variance explained an average of 24–35% of the methylation variance, with a number of CpG sites possibly autonomous from genetic control. We also detected both cis- and trans-meQTLs, with only trans-meQTLs overlapping with previously identified genomic regions of high differentiation between marine and freshwater ecotypes. Finally, we identified the genetic architecture underlying two key CpG sites that were differentially methylated between ecotypes. These findings demonstrate a potential role for DNA methylation in facilitating adaptation to divergent environments and improve our understanding of the heritable basis of population epigenomic variation.

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Evolution of stickleback spines through independent cis-regulatory changes at HOXDB

10.1101/2021.12.14.472698 ◽

2021 ◽

Author(s):

Julia I Wucherpfennig ◽

Timothy R Howes ◽

Jessica N Au ◽

Eric H Au ◽

Garrett A Roberts Kingman ◽

...

Keyword(s):

Gene Expression ◽

Evolutionary Biology ◽

Gasterosteus Aculeatus ◽

Molecular Mechanisms ◽

Wild Populations ◽

Gene Variation ◽

Regulatory Changes ◽

Fundamental Goal ◽

Apeltes Quadracus ◽

Genetic Mechanisms

Understanding the genetic mechanisms leading to new traits is a fundamental goal of evolutionary biology. We show that HOXDB regulatory changes have been used repeatedly in different stickleback fish species to alter the length and number of bony dorsal spines. In Gasterosteus aculeatus, a variant HOXDB allele is genetically linked to shortening an existing spine and adding a spine. In Apeltes quadracus, a variant allele is associated with lengthening an existing spine and adding a spine. The alleles alter the same conserved non-coding HOXDB enhancer by diverse molecular mechanisms, including SNPs, deletions, and transposable element insertions. The independent cis-acting regulatory changes are linked to anterior expansion or contraction of HOXDB expression. Our findings support the long-standing hypothesis that natural Hox gene variation underlies key morphological patterning changes in wild populations and illustrate how different mutational mechanisms affecting the same region may produce opposite gene expression changes with similar phenotypic outcomes.

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An ecological explanation for hyperallometric scaling of reproduction

10.1101/2021.03.12.435090 ◽

2021 ◽

Author(s):

Tomos Potter ◽

Anja Felmy

Keyword(s):

Body Size ◽

Reproductive Output ◽

Resource Competition ◽

Natural Populations ◽

Scaling Exponent ◽

Wild Populations ◽

Wet Season ◽

Size Dependent ◽

In The Wild ◽

The Relationship

AbstractIn wild populations, large individuals have disproportionately higher reproductive output than smaller individuals. We suggest an ecological explanation for this observation: asymmetry within populations in rates of resource assimilation, where greater assimilation causes both increased reproduction and body size. We assessed how the relationship between size and reproduction differs between wild and lab-reared Trinidadian guppies. We show that (i) reproduction increased disproportionately with body size in the wild but not in the lab, where effects of resource competition were eliminated; (ii) in the wild, the scaling exponent was greatest during the wet season, when resource competition is strongest; and (iii) detection of hyperallometric scaling of reproduction is inevitable if individual differences in assimilation are ignored. We propose that variation among individuals in assimilation – caused by size-dependent resource competition, niche expansion, and chance – can explain patterns of hyperallometric scaling of reproduction in natural populations.

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Genome-wide characterization of genetic diversity and population structure of Valeriana officinalis L.

10.21203/rs.2.10069/v1 ◽

2019 ◽

Author(s):

Maja Boczkowska ◽

Katarzyna Bączek ◽

Olga Kosakowska ◽

Anna Rucińska ◽

Wiesław Podyma ◽

...

Keyword(s):

Population Structure ◽

Population Genomics ◽

Natural Populations ◽

Valeriana Officinalis ◽

Wild Populations ◽

Genetic Fingerprint ◽

Genome Wide ◽

Species Population ◽

Outcrossing Species

Abstract Background: Valeriana officinalis L. is one of the most important medicinal plant with a mild sedative, nervine, antispasmodic and relaxant effect. Despite a substantial number of studies on this species, population genomics has not yet been analyzed. The main aim of this study was: characterization of genetic variation of natural populations of V. officinalis in Poland and comparison of variation of wild populations and the cultivated form using Next Generation Sequencing based DArTseq technique. We also would like to establish foundations for genetic monitoring of the species in the future and to develop genetic fingerprint profile for samples deposited in gene bank and in natural sites in order to assess the degree of their genetic integrity and population structure preservation in the future.Results: The major and also the most astounding result of our work is the low level of observed heterozygosity of individual plants from natural populations despite the fact that the species is widespread in the studied area. Inbreeding, in naturally outcrossing species such as valerian, decreases the reproductive success. The analysis of the population structure indicated the potential presence of metapopulation in a broad area of Poland and the formation of a distinct gene pool in Bieszczady Mountains. The results also indicate the presence of individuals of the cultivated form in natural populations in the region where the species is cultivated for the needs of the pharmaceutical industry and this could lead to structural and genetic imbalance in wild populations.Conclusions: The DArTseq technology can be applied effectively in genetic studies of V. officinalis. The genetic variability of wild populations is in fact significantly lower than assumed. Individuals from the cultivated population are found in the natural environment and their impact on wild populations should be monitored.

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Two different epigenetic pathways detected in wild three-spined sticklebacks are involved in salinity adaptation

10.1101/649574 ◽

2019 ◽

Cited By ~ 2

Author(s):

Melanie J. Heckwolf ◽

Britta S. Meyer ◽

Robert Häsler ◽

Marc P. Höppner ◽

Christophe Eizaguirre ◽

...

Keyword(s):

Natural Selection ◽

Gasterosteus Aculeatus ◽

Natural Populations ◽

Wild Populations ◽

Epigenetic Marks ◽

Transgenerational Plasticity ◽

The Face ◽

Adaptation Processes ◽

Methylation Patterns ◽

Rapid Emergence

AbstractWhile environmentally inducible epigenetic marks are discussed as one mechanism of transgenerational plasticity, environmentally stable epigenetic marks emerge randomly. When resulting in variable phenotypes, stable marks can be targets of natural selection analogous to DNA sequence-based adaptation processes. We studied both postulated pathways in natural populations of three-spined sticklebacks (Gasterosteus aculeatus) and sequenced their methylomes and genomes across a salinity cline. Consistent with local adaptation, populations showed differential methylation (pop-DMS) at genes enriched for osmoregulatory processes. In a two-generation experiment, 62% of these pop-DMS were insensitive to salinity manipulation, suggesting that they could be stable targets for natural selection. Two-thirds of the remaining inducible pop-DMS became more similar to patterns detected in wild populations from the corresponding salinity, and this pattern accentuated over consecutive generations, indicating a mechanism of adaptive transgenerational plasticity. Natural DNA methylation patterns can thus be attributed to two epigenetic pathways underlying the rapid emergence of adaptive phenotypes in the face of environmental change.

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Mhc polymorphisms fail to explain the heritability of phytohaemagglutinin-induced skin swelling in a wild passerine

Biology Letters ◽

10.1098/rsbl.2009.0435 ◽

2009 ◽

Vol 5 (6) ◽

pp. 784-787 ◽

Cited By ~ 11

Author(s):

Camille Bonneaud ◽

Janet S. Sinsheimer ◽

Murielle Richard ◽

Olivier Chastel ◽

Gabriele Sorci

Keyword(s):

Genetic Variation ◽

Immune Responses ◽

Environmental Effects ◽

Natural Populations ◽

Wild Populations ◽

Genetic Determinants ◽

House Sparrows ◽

Additive Genetic Variation ◽

Significant Heritability ◽

Mhc Polymorphisms

Genetic estimates of the variability of immune responses are rarely examined in natural populations because of confounding environmental effects. As a result, and because of the difficulty of pinpointing the genetic determinants of immunity, no study has to our knowledge examined the contribution of specific genes to the heritability of an immune response in wild populations. We cross-fostered nestling house sparrows to disrupt the association between genetic and environmental effects and determine the heritability of the response to a classic immunological test, the phytohaemagglutinin (PHA)-induced skin swelling. We detected significant heritability estimates of the response to PHA, of body mass and tarsus length when nestlings were 5 and 10 days old. Variation at Mhc genes, however, did not explain a significant portion of the genetic variation of nestling swelling to PHA. Our results suggest that while PHA-induced swelling is influenced by the nest of origin, the importance of additive genetic variation relative to non-additive genetic variation and the genetic factors that influence the former in wild populations still need to be identified for this trait.

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Persistent and plastic effects of temperature on DNA methylation across the genome of threespine stickleback ( Gasterosteus aculeatus )

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.1667 ◽

2017 ◽

Vol 284 (1864) ◽

pp. 20171667 ◽

Cited By ~ 32

Author(s):

David C. H. Metzger ◽

Patricia M. Schulte

Keyword(s):

Dna Methylation ◽

Time Scales ◽

Gasterosteus Aculeatus ◽

Natural Populations ◽

Thermal Response ◽

Thermal Acclimation ◽

Threespine Stickleback ◽

Multiple Time Scales ◽

Acclimation Temperature ◽

Multiple Time

Epigenetic mechanisms such as changes in DNA methylation have the potential to affect the resilience of species to climate change, but little is known about the response of the methylome to changes in environmental temperature in animals. Using reduced representation bisulfite sequencing, we assessed the effects of development temperature and adult acclimation temperature on DNA methylation levels in threespine stickleback ( Gasterosteus aculeatus ). Across all treatments, we identified 2130 differentially methylated cytosines distributed across the genome. Both increases and decreases in temperature during development and with thermal acclimation in adults increased global DNA methylation levels. Approximately 25% of the differentially methylated regions (DMRs) responded to both developmental temperature and adult thermal acclimation, and 50 DMRs were common to all treatments, demonstrating a core response of the epigenome to thermal change at multiple time scales. We also identified differentially methylated loci that were specific to a particular developmental or adult thermal response, which could facilitate the accumulation of epigenetic variation between natural populations that experience different thermal regimes. These data demonstrate that thermal history can have long-lasting effects on the epigenome, highlighting the role of epigenetic modifications in the response to temperature change across multiple time scales.

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There Is No Evidence of Geographical Patterning among Invasive Kentucky Bluegrass (Poa pratensis) Populations in the Northern Great Plains

Weed Science ◽

10.1614/ws-d-15-00169.1 ◽

2016 ◽

Vol 64 (3) ◽

pp. 409-420 ◽

Cited By ~ 2

Author(s):

Lauren A. Dennhardt ◽

Edward S. DeKeyser ◽

Sarah A. Tennefos ◽

Steven E. Travers

Keyword(s):

Genetic Diversity ◽

Great Plains ◽

Propagule Pressure ◽

Poa Pratensis ◽

Natural Populations ◽

Kentucky Bluegrass ◽

Grass Species ◽

Northern Great Plains ◽

Wild Populations ◽

High Genetic Diversity

The study of colonizing and of dominant grass species is essential for prairie conservation efforts. We sought to answer how naturalized Kentucky bluegrass in the northern Great Plains has become successful in the last 20 yr despite its long history in the northern Great Plains. We tested for evidence of geographical differentiation using flow cytometry and microsatellite markers to ascertain the population genetics of Kentucky bluegrass. Across all tested wild populations, high levels of genetic diversity were detected along with moderate levels of structure. Mantel tests of geographical patterns were not significant. Using clonal assignment, we found two major clones that made up the majority of the tested wild populations. When we compared the wild individuals to pedigree cultivars, we found virtually no genetic overlap across all tests, which did not support our hypothesis of developed cultivars contributing to high genetic diversity in natural populations. Furthermore, DNA content tests indicated a narrow range in ploidy in wild populations compared with lawn cultivars, further supporting a hypothesis of divergence between wild and pedigree cultivars. These results indicate the recent invasion of Kentucky bluegrass in the northern Great Plains is not because of adaptation or propagule pressure, but rather likely an environmental or land use shift.

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