Geneticists dig up the dirt on 300 years of succulence.

When Steve Knapp started his new job at the University of California, Davis, he plunged into a forensic mystery that would take years to unravel. He wasn’t hunting a criminal or identifying a missing person, but the challenge before him was just as formidable: reconstructing the genetic identity of more than one thousand strawberry plants owned by the university. In the end, the strawberry genealogy would expand to include over 8,000 individuals around the world.

Knapp is director of the Strawberry Breeding Program at UC Davis. The humble strawberry, that ubiquitous staple of summer picnics, represents big business for the University of California. Strawberries bred at UC Davis account for around half of California’s $2.6 billion annual crop. “In the entire UC system, for many years, it was the top royalty generator,” said Knapp. While pharmaceuticals have now taken the lead, licensing fees from the berries still bring in more than $7 million a year.

UC Davis hired Knapp in 2015 to restore confidence in their strawberry breeding program after the previous director left to start his own private breeding company. Fearing the program would be shuttered, the California Strawberry Commission (CSC) sued the school. Knapp was brought on board as part of the university’s settlement with the CSC, reinforcing the program’s commitment to continue producing new strawberry varieties.

Knapp faced a massive challenge. To successfully breed the plants, he had to know what the program’s historic collection contained, but some 95% of the pedigree records were missing. With around 1,500 specimens and sparse records, he and his team would need to draw on a combination of molecular genetic techniques and old-fashioned genealogical detective work to document the collection.

Now published in G3: Genes|Genomes|Genetics, this huge curation project also explored the tangled roots of today’s strawberries. Modern varieties were first created in 18^th century France from spontaneous crosses between the Chilean strawberry and another New World import, the Virginian strawberry. After the mysterious parentage of these cultivars was uncovered by a teenage botanist working in the palace gardens of Versailles, horticulturalists developed the fruit into the large berries recognizable to shoppers today.

But this long-told origin story glosses over the true complexity of the modern strawberry’s ancestry. Over the years, breeders intensively crossed, back-crossed, and selected countless varieties from across the world, repeatedly introducing various wild species into the mix. The genetic twists and turns of strawberry domestication are still not fully understood.

To map the relationships between specimens in the university collection, the team used high-density single nucleotide polymorphism (SNP) genotype analysis. They genotyped every individual plant in the collection and applied statistical analyses to establish parent-offspring relationships. The pedigrees that they generated—replete with long-lived individuals, overlapping generations, and extensive hybridization—became too large and complex for conventional pedigree visualization software, so the researchers turned to tools for social network analysis to identify patterns and relationships between the plants. This method enabled them to visualize the diversity of individual plants that have “founded” domesticated populations over the 300-year history of strawberry cultivation.

To delve beyond the Davis collection, Knapp posed a challenge to the members of his lab. “I said, it would be really cool to connect this UC material to the founders that created it,” he said. “Where did that material come from?”

Graduate student Dominique Pincot sank her teeth into the project. She followed the paper trail to the University of Utah, where she found a set of notebooks containing pedigrees recorded by Royce Bringhurst, “Mr. Strawberry,” who headed the UC Davis program from 1952 to 1989.

Next, the team tracked down pre-WWII pedigrees from the UC collection that had made their way to Driscoll Strawberry Associates, the commercial berry seller. “We literally had these three-ring binders full of crusty old notes of pedigrees that gave us a pretty good reconstruction all the way back to the early Berkeley days,” Knapp said.

Each new thread led to another set of records, and Pincot continued tracing various lineages back through North American and European records and catalogs. The project amassed over 800 sources of data documenting the genealogy of today’s strawberry varieties, and the pedigree encompassed 8,851 individual plants.

“We eventually translated this from this massive legal battle into a labor of love,” Knapp said. “It became extremely fun for us.”

Besides the practical benefit to the UC Davis breeding program, the strawberry genealogy project provides broader scientific benefits. Understanding how modern strawberry genetics relates to earlier varieties is informative because agricultural cultivation often reduces genetic variation within a species. Ultimately a lack of diversity from too much inbreeding can harm the health of the species as well as limiting the options for introducing new traits. Knapp’s analysis revealed that although more than 80% of ancestor strawberries are now extinct, the modern strawberries have retained a great deal of genetic diversity from those ancestors.

Additionally, the project shed light on the breeding speed of the strawberry, or the number of years between generations. “We showed that the breeding cycle was fairly long,” said Knapp. “We made the argument that genetic gains can be increased by speeding it up.” The breeding cycle has decreased over the last 200 years from nearly 17 years per generation down to about six. Faster breeding times would enable the introduction of more genetic variation.

Having this genealogical information to hand has already enabled new kinds of strawberry genomic analysis and tool development. It also advances predictive breeding, a method that uses genetic information to forecast which offspring will have desired traits. “This project was meant to tell us, how did we get here and where have we been, and how can we use this information to predict the future,” said Knapp.

CITATION

Social network analysis of the genealogy of strawberry: retracing the wild roots of heirloom and modern cultivars

Dominique D A Pincot, Mirko Ledda, Mitchell J Feldmann, Michael A Hardigan, Thomas J Poorten, Daniel E Runcie, Christopher Heffelfinger, Stephen L Dellaporta, Glenn S Cole, Steven J Knapp

G3 Genes|Genomes|Genetics, Volume 11, Issue 3, March 2021, jkab015, https://doi.org/10.1093/g3journal/jkab015

Crop properties improved by point mutation in microRNA binding domain of Q gene.

Humans have been cultivating wheat for ten thousand years, transforming it from an unruly grass into a useful crop highly adapted to our needs. But even after millennia, there are still new avenues for improving this staple food.

A new type of common bread wheat (Triticum aestivum L.) was recently discovered that has properties that could improve the way it bakes, such as an elevated grain protein content. Researchers at Sichuan Agricultural University found that the new variety has a mutation in the gene Q, which was already identified as an important player in wheat’s domestication.

Q’s expression is normally negatively regulated by an miRNA that binds and cleaves its mRNA, preventing it from being translated into protein. The new type of wheat has a point mutation in Q’s miRNA binding domain, which disrupts normal regulation. A good match between the miRNA sequence and its target sequence in the mRNA is needed for binding and, thus, cleavage, so this single mutation in the binding site can have major consequences. Xu et al. confirmed that the mutant plants do, in fact, overexpress Q for this very reason.

Left: Bread made with the new wheat variety. Right: Bread made with wild-type wheat.

These results are an important step toward a better grasp on how Q can be manipulated to improve one of the world’s most important crops. The mutant wheat has a substantial advantage over wild-type wheat; for example, the loaf volume of bread produced with the mutant wheat was 37% greater. This work is also significant because it adds another example to the growing list of miRNA functions in plants. These regulators are now thought to be critical for a huge variety of biological processes in plants, but for many miRNAs, we lack the type of mechanistic information this study provides.

CITATION:

An Overexpressed Q Allele Leads to Increased Spike Density and Improved Processing Quality in Common Wheat (Triticum aestivum)
Bin-Jie Xu, Qing Chen, Ting Zheng, Yun-Feng Jiang, Yuan-Yuan Qiao, Zhen-Ru Guo, Yong-Li Cao, Yan Wang, Ya-Zhou Zhang, Lu-Juan Zong, Jing Zhu, Cai-Hong Liu, Qian-Tao Jiang, Xiu-Jin Lan, Jian Ma, Ji-Rui Wang, You-Liang Zheng, Yu-Ming Wei, Peng-Fei Qi
G3: Genes|Genomes|Genetics 2018 8: 771-778; https://doi.org/10.1534/g3.117.300562
http://www.g3journal.org/content/8/3/771

Although foxes look cuddly, these wild animals are equipped with sharp bites—and temperaments to match. Fear not, however, if you’re dying to get close to theses fluffy foxes: a nearly 60-year-old experiment has produced a line of them that are friendly enough to pet.  

The process of creating these tame foxes mirrors the way dogs are thought to have been domesticated from their wild wolf ancestors. These friendly foxes have altered hormone balances, and many of them have dog-like changes in appearance, such as white spotting and curled tails. In a report published in G3: Genes|Genomes|Genetics, Hekman et al. delve into the genetics of these tame foxes, taking a detailed look at their brains.

The tame foxes are the result of a famous experiment started at the Institute of Cytology and Genetics in Siberia, in which the animals were selectively bred for traits like agreeability. For comparison, a line of more aggressive foxes was also bred so that differences between the two groups could illuminate the usually slow processes of domestication.

Levels of the stress hormone cortisol are much lower in the blood of tame foxes than in the aggressive animals. “The question that was really driving me was: What’s different in the brain?” says Jessica Hekman, lead author of the study.

Hekman and her colleagues used RNA sequencing to measure gene expression in the pituitary glands of tame and aggressive foxes. They were interested in the pituitary because it is vital in coordinating the release of many hormones—including cortisol.

The researchers found that genes related to exocytosis were differentially expressed, which suggests the cells could be secreting neurotransmitters and hormones to the blood differently in the two lines. Given the differing levels of blood cortisol observed, this wasn’t all that surprising.

Some other differentially expressed genes were more unexpected, however. “I kept finding a bunch of genes related to pseudopodia, which was a huge surprise,” Hekman recalls. Pseudopodia are cellular protrusions best known for driving movement in single-celled organisms—think of how an amoeba moves by extending its cellular membrane. Cells in the brain aren’t mobile in the same sense, but pituitary cells use pseudopodia to coordinate with each other and move closer to blood vessels for hormone release. This study suggests that pseudopodia function differently in the pituitary glands of tame foxes than in aggressive ones. Hekman explains that this makes a lot of sense because tame and aggressive foxes actually produce similar amounts of hormones in the pituitary gland—the critical difference is in the amount that is released into the bloodstream.

Hekman is optimistic that a better understanding of these differences in foxes might reveal more about what’s going on in aggressive pets. A better understanding of the biological underpinnings of aggression could even have implications for the development of behavioral medication in the future. “It’s a correlational study; it’s a first step,” says Hekman, “The next step is to get living cells and put them through functional tests.” Though the study is an early investigation, it opens doors for future work that might point toward a pill for your pugnacious pup.

CITATION

Anterior Pituitary Transcriptome Suggests Differences in ACTH Release in Tame and Aggressive Foxes

Humans built the modern world with the help of domestic plants and animals. A byproduct of our many domestication experiments is a series of excellent long-term controlled evolutionary comparisons that are helping geneticists understand adaptation. In a study published in the May issue of G3, Fleming et al. identify genomic regions under natural selection in indigenous African and European chicken populations that optimize survival in these very different environments.

Commercially raised chickens have been bred to thrive in the highly controlled environment of modern farms, but domesticated chickens have been living with humans in different regions across the globe for thousands of years. Heritage chicken breeds that are specific to certain geographic areas still carry the traits selected for in their ancestors that allow them to survive in harsher conditions. The authors of this study chose collections of such chickens from Northern Europe, where farm animals must endure cold and snow, and from Africa and the Middle East, where extremely high temperatures are the main obstacle for survival.

After genotyping a large sample of African and European chickens at a selection of SNPs across the whole genome, they used patterns of variation to identify regions associated with the ability to survive stressful temperatures. They found large genomic regions on three different chromosomes that were significantly different between the two populations of chickens and looked at variation within the groups to identify genomic regions that appeared to be under selection.

The authors found different genome regions were under selection in African and European chickens, showing that the basis of adaptation to these very different environments is genetically distinct. In African chickens, a large region on chromosome 27 stood out as significant in all analyses. This region includes several genes that have been previously implicated in heat stress responses in other animals. Some are linked to heart function and blood vessel formation, which may help these animals thrive in high temperatures.

In Northern European chickens, significant regions were scattered across several chromosomes, with one large region on chromosome 2. One gene in this area has been shown to alter feathering patterns, suggesting that changes to the birds’ plumage might give them an advantage in the cold through improved ventilation or insulation. Additional candidate genes linked to insulin secretion and other metabolic activities suggest that energy regulation could promote the ability to tolerate cold.

Though the birds in this study are not maintained commercially, understanding what makes them suited to their environments may have important implications for mainstream chicken farmers. Current commercial chickens are more susceptible to environmental stress than these distant relatives, and the threat of climate change means they may have to adapt quickly.

CITATION

Genomic Comparison of Indigenous African and Northern European Chickens Reveals Putative Mechanisms of Stress Tolerance Related to Environmental Selection Pressure

Damarius S. Fleming, Steffen Weigend, Henner Simianer, Annett Weigend, Max Rothschild, Carl Schmidt, Chris Ashwell, Mike Persia, James Reecy and Susan J. Lamont

G3: Genes, Genomes, Genetics May 1, 2017 vol. 7 no. 5 1525-1537; https://doi.org/10.1534/g3.117.041228

http://www.g3journal.org/content/7/5/1525

Whether a thunderclap drives your dog to cower behind the couch or leaves it unfazed may be determined in part by genetics. In the June issue of GENETICS, Ilska et al. analyze genetic contributors to canine personality traits—such as fear of loud noises—using owners’ reports of their pets’ behavior.

The researchers chose this survey-based method in place of standardized behavior testing both to create a large body of data and to eliminate any influence of a foreign testing environment on the dogs’ behavior. They measured 12 different traits, from trainability to tendency to bark, using a 101-item questionnaire called the Canine Behavioral Assessment and Research Questionnaire (C-BARQ) that was originally designed to screen potential guide dogs. Then they looked for relationships between these traits and aspects of the dogs’ pedigrees and genotypes.

Of these traits, the most heritable were fear of noises and ability to play fetch. Perhaps surprisingly, many of the genetic factors linked to fetching ability were not related to other aspects of trainability. Aggression toward strangers and other dogs was also heritable, but aggression toward owners was not, likely because humans have placed strong selective pressure on dogs to be loyal and gentle toward their owners, leading to low genetic variance. Some traits were also related to each other—trainability had an inverse relationship with “unusual behavior,” a finding that probably wouldn’t shock most dog owners.

Some of the variants associated with the personality traits were located near genes with known neurological functions. For example, dogs that were prone to agitation often carried a variant near the gene for tyrosine hydroxylase, which is involved in the synthesis of the neurotransmitter dopamine. In humans, dopamine dysfunction is implicated in psychological conditions such as attention deficit-hyperactivity disorder, and some variants of the tyrosine hydroxylase gene are associated with the tendency to experience negative emotions and excitability—both traits related to impulsivity.

Because the study was conducted only on Labrador Retrievers in the United Kingdom, the authors caution that other dog breeds may differ in how heritable different personality traits are. But in any case, just like human personalities, it seems that dog personalities have a strong genetic component. So if your dog stares at you blankly next time you throw it a ball, don’t succumb to frustration—fetching just may not be in its genes.

CITATION:

Ilska, J.; Haskell, M.; Blott, S.; Sánchez-Molano, E.; Polgar, Z.; Lofgren, S.; Clements, D.; Wiener, P. Genetic Characterisation of Dog Personality Traits.
GENETICS, 206(2), 1101-1111.
DOI: 10.1534/genetics.116.192674
http://www.genetics.org/content/206/2/1101

Like any revolutionary technology, domestic horses changed human society. The incredible speed and strength of these animals opened up new opportunities to spread trade, language, and culture. For thousands of years, horses have been helping build human society by pulling wagons and plows and carrying soldiers and travelers on their backs. Horse husbandry changed humanity, but along the way we changed horses too.

A new review paper by Pablo Librado and colleagues in the October issue of Genetics tells the story of how the modern horse came to be. They track the genetic changes that led from wild horses living on the Eurasian steppes 5,500 years ago to the many highly specialized breeds of domestic horse that exist today.

Modern horses have been shaped into distinct breeds with different talents and specialties. Compare a racing thoroughbred with a draft horse like a Clydesdale —they’re extremely different animals now, but they both descend from the same ancestral group of wild horses. Comparing the DNA variation of all different kinds of domestic horses and their only living wild relative, Przewalski’s horse, can reveal the genetic changes that occurred during domestication. Librado and colleagues emphasize that another crucial tool used for tracing the horse lineage is ancient DNA, which is extracted from bones of animals that have been dead for thousands of years. The oldest successfully extracted DNA came from the skeleton of a wild horse that lived in the Yukon between 560,000 – 780,000 years ago. Such samples are especially important because there are very few wild horses left alive, and modern horse breeding practices have obscured the genomic signature of early domestication qualities like geography. Thanks to data from ancient DNA, geneticists have learned that a previously unknown group of now-extinct wild horses were also ancestors to modern horses.

Remarkably, the majority of Y-chromosomes carried by modern domestic horses can be traced back to just a few stallions. This could be because only a few males were originally used in domestication, but it could also result from carefully controlled modern breeding practices where a single male sires a huge number of offspring. The ultimate cause of this very low Y-linked diversity is still debated, but strict selective breeding has almost certainly contributed. In contrast, a much larger number of females than males contributed ancestry to domestic horses. According to Librado and colleagues, it seems that wild mares were continuously introduced into human-controlled herds throughout the process of domestication.

Turning a wild animal into a domestic one that will tolerate humans involves a long process of selecting for traits like docility and friendliness. In the case of hard-working horses, desirable traits also included strength, endurance, and gait. This kind of selective breeding leaves a very clear mark in the genome.  By comparing the genomes of modern domestic horses with very ancient domestic horses, geneticists were able to identify many genes linked to selected traits, including genes involved in coat color, skeletal structure, the circulatory system, and brain development and behavior.

Photo by Softeis via Wikimedia. The speed and stamina of modern racing thoroughbreds are the results of extensive artificial selection.

Similarly, comparing modern breeds can identify the genes that make each breed so different. Librado and colleagues describe how scientists have used this approach to identify gene variants involved in the superior racing ability of thoroughbreds and alternative gaits like those used in competitive jumping and dressage. Lesser known traits have also been investigated, like extreme cold tolerance in Yakutian horses. Their ability to survive harsh Siberian winters has been linked to genome regions that influence coat hair density and metabolism. Many domestic breeds suffer from a high frequency of inherited illnesses due to harmful gene variants being inadvertently selected alongside a beneficial trait. Genetic work has identified the genetic cause of muscle defects in Belgian draft horses, which interestingly enough may have once been a beneficial trait under the harsher conditions of its working past.

In many ways, understanding the history of horses is a vital part of understanding our own story. Yet many traditional horse breeds are now endangered, and unanswered questions about the genetics of horse domestication remain. In this review, Librado and colleagues urge haste to conserve this source of unique variation before it is too late.

Librado, P., Fages, A., Gaunitz, C., Leonardi, M., Wagner, S., Khan, N., Hanghøj, K., Alquraishi, S., Alfarhan, A., Al-Rasheid, K., Der Sarkissian, C., Schubert, M., & Orlando, L. (2016). The Evolutionary Origin and Genetic Makeup of Domestic Horses. Genetics, 204(2), 423-434. DOI:10.1534/genetics.116.194860

http://www.genetics.org/content/204/2/423.article-info

A genomic analysis of 28 dog breeds has traced the genetic history of the remarkable Fonni’s Dog, a herd guardian endemic to the Mediterranean island of Sardinia. The results, published in this month’s issue of GENETICS, reveal that the regional variety has developed into a true breed through unregulated selection for its distinctive behavior, and that its ancestors came from the very same geographic areas as Sardinia’s human migrants. Just as Sardinian people have long provided a wealth of genetic insights to scientists, the canine natives are an example of an isolated population that could prove a powerful resource for finding genes that influence health and behavior.

Fonni’s Dogs (Cane Fonnese in Italian) are large, rugged dogs known for their wariness towards strangers and their intense facial expression. Although there are descriptions of these shephard’s companions dating to at least the mid-nineteenth century, it is not officially recognized as a breed by most international registries, including the largest federation of kennel clubs, the Federation Cynologique Internationale.

“If you were to look at ten Fonni’s Dogs, you would see there’s a lot of variation in coat color and fur length. But they are all good protectors of their flocks. That’s because nobody cares what they look like; they’ve been bred to do a job and to do it right,” says study leader Elaine Ostrander of the National Human Genome Research Institute (NHGRI).

The Fonni’s Dog (Cane Fonnese or Sardinian Sheepdog) is endemic to Sardinia and is known for its fiercely protective guarding behaviors. Photo credit: Stefano Marelli

That job is guarding the possessions of their owner, to whom they are fiercely loyal. “Fonni’s are also outstanding thieves,” says Ostrander. “They can be trained to sneak over to the neighbors’ and bring items home.” While this particular duty isn’t required by today’s Fonni Dogs, written records from the mid-1800’s indicate that thievery was part of their historical repertoire.

The island home of the Fonni’s Dog has long held the interest of geneticists. Because Sardinia is geographically isolated, its human inhabitants share a unique ancestry and relatively low genetic diversity. Those characteristics make it easier to study genetic influences on disease and aging in Sardinians than in other human groups. Ostrander and other canine geneticists argue that each of the hundreds of different dog breeds also represents an isolated population that could be harnessed for genetic studies.

“Dogs get all the same diseases as humans, and there are lots of dog breeds with genetic predispositions, for example to particular types of cancer,” Ostrander says. “Once we understand the genetic history of a breed we can search for disease genes in a much more powerful way than is possible in humans, enabling us to hone in on medically-relevant genes.”

To better understand how the Fonni’s Dog developed, scientists from the NHGRI, the University of Milan, and G. d’Annunzio University analyzed blood samples from Fonni’s Dogs living in different parts of Sardinia and sequenced the whole genome of one of these dogs. To trace the Fonni’s relationship to dogs from around the Mediterranean, the team compared the data to DNA from 27 other European, Middle Eastern, and North African breeds.

This diagram indicates the geographic origin of the 28 dog breeds studied. Abbreviations: Anatolian Shepherd, ANAT; Azwahk Hound, AZWK; Berger Picard, BPIC; Bouvier des Flandres, BOUV; Cane Corso, CANE; Cane Paratore, CPAT; Cirneco dell’Etna, CIRN; Fonni’s Dog, FONN; Great Pyrenees, GPYR; Ibizan Hound, IBIZ; Istrian Shorthaired Hound, ISHH; Italian Greyhound, ITGY; Komondor, KOMO; Lagotto Romagnolo, LAGO; Levriero Meridionale, LVMD; Maltese, MALT; Mastino Abruzzese, MAAB; Neapolitan Mastiff, NEAP; Pharaoh Hound, PHAR; Portuguese Water Dog, PTWD; Saluki, SALU; Sloughi, SLOU; Spanish Galgo, GALG; Spanish Water Dog, SPWD; Spinone Italiano, SPIN; Standard Schnauzer, SSNZ; St Bernard, STBD; Volpino Italiano, VPIN.

The data revealed that the Fonni’s dog shows all the genetic hallmarks of being a breed, even though it developed in the absence of a regulated pedigree program and only arose through the tendency of Sardinian shepherds to choose their best guard dogs for breeding. The researchers compared individual dogs from within the same breed and across different breeds, quantifying many aspects of genome variation and genetic distinctiveness. All these measures confirmed that the Fonni’s Dog, in genetic terms, is a breed.

The study also revealed the ancestors of the Fonni’s Dog were related to the Saluki, a swift and graceful “sight” hound from the Near and Middle East, and a large mastiff like the Komondor, a powerfully-built sheep guardian from Hungary that looks a bit like a mop.

Strikingly, the origins of the Fonni’s Dog mirror human migration to Sardinia. Studies of the island’s human inhabitants have shown they share greatest genetic similarity with people from Hungary, Egypt, Israel, and Jordan. “The map we can draw of the dog’s origins is the same as the map of human migration to Sardinia,” says Ostrander. “Clearly ancient people traveled with their dogs, just as they do now.”

The close parallels between the history of the dog and human inhabitants of the island has a practical implication, says Ostrander. “Our study shows how closely dog migration parallels human migration. It could be that if you have missing pieces in a study of a human population’s history, samples collected from dogs in the right place could fill in those gaps.”

Smooth-coated (left) and rough-coated (right) varieties of Fonni’s Dog. Genetic analysis confirms the varied appearance of the Fonni’s Dog masks the underlying unity of the breed. Photo credit: Luca Spennacchio

The team plans next to study in greater detail eleven regions of the genome that likely make the Fonni’s Dog distinct — these may be responsible for their characteristically loyal and protective behavior.

Ostrander points out the study was a collaborative effort with scientists from Italy, including Sardinia, and says she is gratified to find so many researchers across the world interested in similar questions. Her group is hoping to work with colleagues in a range of countries to explore other so-called “niche” dog populations, regional varieties that often have a history of being bred for a particular job. Their goals are to better understand how dogs have evolved and to demonstrate yet another important job for these faithful human companions: tracking down disease genes.

CITATION

Commonalities in Development of Pure Breeds and Population Isolates Revealed in the Genome of the Sardinian Fonni’s Dog

Dayna L. Dreger, Brian W. Davis, Raffaella Cocco, Sara Sechi, Alessandro Di Cerbo, Heidi G. Parker, Michele Polli, Stefano P. Marelli, Paola Crepaldi, Elaine A. Ostrander

GENETICS October 1, 2016 vol. 204 no. 2 737-755;

http://www.genetics.org/content/204/2/737

DOI: 10.1534/genetics.116.192427

The mild temperament that distinguishes the family dog from its wolf ancestors is just one of a whole array of traits that seem to have evolved during domestication. Domestication syndrome refers to the suite of characteristics commonly observed in domestic animals, including docility, shorter muzzles, smaller teeth, smaller and floppier ears, and an altered estrous cycle. Some work has suggested that these characteristics are linked to neural crest cell deficits during embryonic development, and research featured in the August issue of G3 has revealed a possible mechanism.

The researchers discovered that free-breeding dogs, whose mating has not been carefully managed by humans, had several genetic differences from pure-breed types of both East Asian and European origin. The dogs differed in genes involved in development, metabolism, the nervous system, and behavior—all traits affected by domestication. Prior research uncovered similar categories of genes with signatures of selection between dogs and gray wolves, implying that the comparison between free-breeding and pure-breed dogs can provide insights into the effects of artificial selection (resulting from the regulation of dog breeding by humans), whether it occurred in the very earliest or later stages of domestication.

Surprisingly, the researchers noticed that several of the affected genes are linked to each other by the Hedgehog signaling pathway, which is a major contributor to development of bones, the skull, muscles, brain, sex organs, neurons, and olfactory pathways. Perhaps most intriguingly, one of the Hedgehog genes, called Sonic Hedgehog, inhibits adhesion and migration of neural crest cells from their source, the neural tube, by providing positional cues. In vertebrates, the same gene regulates craniofacial development, a process that is strikingly different between dogs and wolves.  

Further supporting the link between domestication and neural crest cell migration, the researchers found that one of the disparities between the pure-breed and free-breeding dogs occurs in a homolog of a gene known to affect neural crest cells. Another candidate gene is involved in the diseases Bardet-Biedl syndrome and McKusick-Kaufman syndrome in humans. People with Bardet-Biedl syndrome often have flattening of the midface and crowded teeth. In mice, deleting this gene disrupts Sonic Hedgehog signaling, causing defects in cranial neural crest cell migration. The end result is a shortened snout—one of the characteristics of domestication syndrome.

These findings suggest that problems with neural crest cells are central to the domestication syndrome. This could explain why dogs’ tameness is accompanied by physical differences that make dogs look distinct from wolves. It’s a two-for-one deal: good behavior and cuteness wrapped up in a single syndrome.

CITATION:
Pilot, M.; Malewski, T.; Moura, A.; Grzybowski, T.; Oleński, K.; Kamiński, S.; Fadel, F.; Alagaili, A.; Mohammed, O.; Bogdanowicz, W. Diversifying Selection Between Pure-Breed and Free-Breeding Dogs Inferred from Genome-Wide SNP Analysis.
G3, 6(8), 2285-2298.
DOI: 10.1534/g3.116.029678
http://www.g3journal.org/content/6/8/2285.long

Sequencing the genomes of hundreds of strains of the wine yeast S. cerevisiae has revealed little genetic diversity and high levels of inbreeding. In many cases, yeast strains sold by different companies were almost genetically identical. The results, published in the April issue of G3: Genes|Genomes|Genetics, suggest that winemakers attempting to develop improved wine yeasts will need to look to creating hybrids with more exotic strains.

“It takes a tough yeast to ferment wine,” says lead author Anthony Borneman of the Australian Wine Research Institute. “Wine yeast need to be far more stress tolerant than strains used in brewing or baking, for example, to cope with the very high sugar and acidity levels of grape juice. Our results show that only a limited branch of the yeast evolutionary tree is currently used in winemaking.”

Yeast contributes to the flavors of wine, and may even provide a component of a wine’s “terroir,” the local conditions that give a wine its unique flavor. Traditionally, wine has been fermented by naturally occurring yeast, but this can deliver inconsistent results from vintage to vintage. To yield more predictable results, most winemakers now use pure active dried yeast starter strains that have been produced by commercial suppliers.

Scientists at the Australian Wine Research Institute are developing new strains of yeast that contribute different flavor profiles during wine fermentation, including boosted floral aromas. To better understand the genetic diversity available for breeding new yeast types, the authors of the study sequenced 212 strains of the yeast Saccharomyces cerevisiae. This included commercial wine and brewing starters and strains isolated from natural fermentations of wine and other alcoholic beverages.

The results showed that virtually all the wine yeasts were closely related and carry only a tiny fraction of the overall pool of S. cerevisiae genetic diversity. For example, most of the strains from the Prise de Mousse collection of champagne yeasts carry almost identical gene variants. These yeasts likely arose from a single ancestor, or from an inbred ancestral population. In fact, dozens of strains sold by different companies are, genetically speaking, almost completely indistinguishable.

None-the-less, subtle genetic distinctions were often detected between strains, which may be responsible for their unique fermentation and flavor properties. There were also a few cases of major differences. For example, four strains carry a unique set of genes involved in producing a class of aromatic chemicals. In another example, several commercial strains seem to be derived by hybridization with non-wine yeast strains, and contain a gene cluster typically associated with ale yeast.

However, the overall picture of diversity means there is limited scope for creating new strains solely from wine yeasts. Instead, gene variants will need to be introduced by hybridization with other diverse strains of S. cerevisiae, says Borneman, such as those found in natural fermentations of African palm wine and other environmental isolates. For instance, the yeasts used to brew the Japanese beverage sake carry genes not found in wine and ale yeasts. These genes allow the yeast to synthesize their own supply of the micronutrient biotin, rather than relying on biotin supplied in their food source.

Besides serving as a resource for winemakers choosing yeast varieties for fermentations and strain development, the genome sequences provide a platform for many types of genetic experiments, including genome-wide tests that can link specific gene variants to particular flavor or fermentation characteristics.

“We hope better understanding of yeast will allow us to tailor these organisms for specific uses, much as we have bred better varieties of domesticated plants and animals over millennia,” says Borneman.

CITATION
Whole Genome Comparison Reveals High Levels of Inbreeding and Strain Redundancy Across the Spectrum of Commercial Wine Strains of Saccharomyces cerevisiae
Anthony R. Borneman, Angus H. Forgan, Radka Kolouchova, James A. Fraser, and Simon A. Schmidt
G3: Genes|Genomes|Genetics April 2016 6:957-971 doi:10.1534/g3.115.025692
http://www.g3journal.org/content/6/4/957.full

On November 11, 1954, Syuiti Mori turned out the lights on a small group of fruit flies. More than sixty years later, the descendents of those flies have adapted to life without light. These flies—a variety now known as “Dark-fly”—outcompete their light-loving cousins when they live together in constant darkness, according to research reported in the February issue of G3: Genes|Genomes|Genetics. This competitive difference allowed the researchers to re-play the evolution of Dark-fly and identify the genomic regions that contribute to its success in the dark.

“We hope understanding the genetics behind Dark-fly’s adaptations will shed light on how genes are selected during rapid evolution,” says study leader Naoyuki Fuse of Kyoto University. The Dark-fly project is the longest-running example of an experimental evolution study where scientists follow a population over many generations. It is also the first to analyze genome evolution in a multicellular organism adapted to a defined condition in the lab.
The project was initiated by Mori as part of a series of experiments investigating how the traits of fruit flies are altered in response to changes in their environment. The fruit fly Drosophila melanogaster is a heavily studied model organism often used to examine genetic changes during evolution. To keep the flies away from light, they are reared in vials kept in a large pot painted black on the inside and covered with a blackout cloth. When the vials and food need to be changed, the researchers tend to the flies in the pitch dark, then use a feeble red light to check on their work. Fruit flies can’t see this light because the species lacks those light receptor proteins that absorb red wavelengths.

When Mori retired, he passed on the precious fly stocks to his colleagues at Kyoto University, who have maintained them continuously to this day. The stock of flies has now spent more than 1,500 generations without light. In human terms, that would be like sequestering generations of our ancestors in the dark for 30,000 years.

Today, Dark-fly looks almost identical to normal (wild-type) D. melanogaster, but the variety is also subtly different. For example, Dark-fly individuals move around more in response to sudden light exposure, even after spending a generation in normal day/night cycles. They are also more sensitive to certain smells and have longer head bristles, which are sensory organs that serve as the fruit fly version of a cat’s whiskers. Dark-fly also produces more offspring when kept in constant darkness than in alternating light and dark.

But although Dark-fly does better in the dark than the light, is it more highly adapted than the wild-type to its dim environment? The team tested this hypothesis by housing the two types of fruit flies together, allowing them to mate at random, and then assessing the parentage of the flies that made up the next generations. The results showed that Dark-fly has a competitive advantage in reproduction over the wild-type when bred in the dark. Fuse suggests this might be due to differences in pheromone signaling when the flies select their mates, or to altered circadian rhythms of mating or sleep behaviors.

Which genes are responsible for the adaptation to dark conditions? Previously, the team sequenced the Dark-fly genome, identifying mutations that distinguish it from wild-type. But not many of those genetic variants are likely to be responsible for the adaptations that help Dark-fly thrive without light; many of the variants may have no effect, or may affect unrelated traits. To hone in on the dark-adaptation genes, the team performed another kind of experimental evolution study.

They first reared Dark-flies and normal flies in mixed colonies, allowing the two types to interbreed freely for 49 generations. These colonies were maintained in constant dark and compared to control colonies with normal 24-hour light/dark cycles. With each generation, those flies that produced the most offspring contributed more of their genes to the colony as a whole. As the genomes of the two types of fly mixed, those genes responsible for Dark-fly’s unique adaptations should become more common in the colony kept in the dark. To find those genes, the team sequenced the genomes of flies at the beginning and end of the experiment and looked for genetic variants originating in Dark-fly that became more common only under the dark conditions.

Such variants were located in 28 regions of the Dark-fly genome. From these regions, the researchers narrowed down the candidates to 84 genes. Among these candidates are likely the genes associated with dark-adaptive traits. These include genes that encode chemical receptors, and genes involved in pheromone synthesis, the formation of smell memories, and circadian rhythms. In future work, the team will examine the activity and functions of these candidates to link them to specific Dark-fly adaptations.

“We will soon have the ability to try my dream experiment: using genome-editing technology to introduce defined mutations into the wild-type to try to reproduce the Dark-fly’s traits. This would give us a precise molecular profile of this remarkable example of evolution in the lab,” says Fuse.

CITATION:

Dynamics of Dark-Fly Genome Under Environmental Selections

Minako Izutsu, Atsushi Toyoda, Asao Fujiyama, Kiyokazu Agata, and Naoyuki Fuse

G3: Genes|Genomes|Genetics February 2016 6: 365-376; doi:10.1534/g3.115.023549

http://www.g3journal.org/content/6/2/365.full

Update added March 7, 2016:

We’ve since learned that GSA member and FlyBook Co-Editor-in-Chief Therese Markow pioneered related research in 1975. During her PhD, she showed the importance of genetic variation in movement towards light (phototaxis) for fitness in constant darkness or constant light. The project relied on a quantitative assay for phototactic behavior: the flies enter a maze where they make a series of 15 consecutive choices between moving towards or away from light. The more phototactic the fly, the more frequently it should choose the light. This allows not only classification of the trait along a spectrum, it provides a framework for systematically creating fly lines with extreme behavior via artificial selection – called “photopositive” and “photonegative” populations. Markow found that photopositive populations laid more eggs in constant light conditions and conversely that photonegative populations laid more eggs under constant darkness. In contrast, unselected flies were mostly unfazed by the light conditions, laying similar numbers of eggs in both cases. This showed that flies have the highest reproductive fitness in the conditions they are genetically programmed to prefer
http://www.nature.com/nature/journal/v258/n5537/abs/258712a0.html