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Three species of fringed sandpiper show feathers during the breeding season, Source: Hennicke Carl, 1902
Editor's Note:
The fringed sandpiper is the only sandpiper that can easily identify its sex during the breeding season. Male fringed sandpipers have a variety of appearances and different ways of attracting females. Scientists have found that a single super gene can determine these differences in male tassel sandpipers through simple Mendelian inheritance.
Compile the | Gu Zhuoya
Editor-in-charge | Chen Xiaoxue
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In late spring and early summer, the birds of the Northern Hemisphere begin to stir. Ruff (Philomachus pugnax), a bird that breeds in northern Eurasia, also changed into gorgeous new clothes and began the annual "Flirting" show.
Male fringed sandpipers have a variety of colors and appearances, some are dressed in noble and domineering black and brown large trunks, some have the snow white fur collar of the Yushu Linfeng, and some have the neutral temperament of weak willow wind. They attract females in different ways in the courtship field.
Male fringed sandpipers have a variety of coat colors, and there are corresponding differences in the "sister-in-law" strategy. Of all male fringed sandpipers, 87-95% are "Independent males" with a variety of black-brown feathers, and they actively defend their courtship territory and show the male king's style.
"Independent" male fringed sandpiper. Image credit: Nature Genetics
White-clad "satellite males" make up only 5-20% of male fringed sandpipers, which are slightly smaller and do not have their own courtship grounds, but because they also have gorgeous costumes, the "independent faction" will allow them to enter the court as their dancing companions to attract more females. The "satellite" fringed sandpiper can also take this opportunity to mate with females.
"Satellite" male fringed sandpiper. Image credit: Nature Genetics
The rare "Faeder male" accounts for less than 1% of male fringed sandpipers, and their "flirting" strategy is also the most special: "Fidel" fringed sandpipers have feathers and body shapes similar to females, and this "neutral" appearance, although it does not directly attract females, allows it to inadvertently blend into the courtship field with other males, confuse competitors, and quietly approach females, thus gaining opportunities.
"Fidel" male fringed sandpiper. Image credit: Nature Genetics
01
Super genes determine complex traits
The colorful fringed plumage and vastly different courtship behaviors of male fringed sandpipers during breeding have attracted attention early on, but what complex genetic mechanisms can lead to so many differences? Two recent papers published in Nature Genetics found astounding results, where these intricate differences can be determined by a simple Mendelian inheritance of a single supergene.
The super gene that controls the differences between the three male tasseled sandpipers is composed of 125 genomes, and this long genetic seat behaves like a whole with three alleles, regulating the coat color, body size and behavior of male fringed sandpipers. Among them, "satellite" and "Fidel" are both explicitly heterozygous, and "independents" are implicitly homozygous. Such a miraculous regulatory mechanism requires that the 125 genes behave like a unified, stable whole, that is, they cannot be recombined frequently across generations.
Researchers such as Sangeet Lamichhaney of Uppsala University in Sweden and Guangyi Fan of the Huada Genetic Research Institute in Shenzhen performed high-throughput sequencing of the genomes of 15 "independent" tassel sandpipers and 9 "satellite" tasseled sandpipers and found that a chromosome about 4.5Mb long was very different between the two types of tasseled sandpipers. Based on this chromosome, phylogenetic analysis of 21 tasseled sandpipers can unambiguously divide the two into two groups, while phylogenetic analysis based on other sequences of the genome cannot separate the two types of tasseled sandpipers. Because this difference is so obvious, the researchers believe that there may be an inversion in this region, that is, a certain section of chromatin is inverted 180 degrees after the two ends are broken and then reconnected. Further experiments proved the existence of inverted positions, with the near-end breakpoint of the invert occurring at 5.8Mb, while the distal breakpoint occurred at 10.3Mb, and there was a 2108bp repeat sequence insertion at the distal inversion.
Lamichhaney pointed out that it is the chromosomal inversion of this locus of the "satellite" and "Fidel" fringed sandpiper that almost completely blocks the recombination of this super gene, resulting in 125 genes behaving as a whole, and the traits of the two can be stablely inherited. The super gene of the "independent" fringed sandpiper due to the absence of this chromosome inversion, there will be a variety of brown-black combinations in the feathers at the neck, while the "satellite" and "Fidel" fringed sandpiper traits are relatively stable.
Since inversion in the supergene occurs in the conserved colinear region of birds, the "independent" tassel sandpiper, which does not exist inversion, should be the most primitive type. The Fidel allelele, which is the largest gap, parted ways with the "independence" allelele about 3.8 million years ago. The "satellite" allele shows a performance between the first two, with one region on the allele closer to the "independent faction" and the other closer to the "Fidel". Researchers believe that the emergence of the "satellite" allele stems from an accidental recombination of the "independent" allelele and the "Fidel" allelele about 500,000 years ago.
In fact, such a result has long been confirmed in morphology, the "satellite" fringed sandpiper neck feather shape is similar to the "independent school", while the smaller size is the same as the "Fidel", indicating that the "satellite" is in between. The "satellite" fringed sandpiper also has its own unique characteristics, such as unique white fringed feathers.
02
Super genes bring death?
However, the wonderful inversion of the super gene does not all bring benefits. One of the breakpoints of the inversion is located in a gene called cenpnant N that encodes the mitoel protein N. Because CENPN plays a key role in the assembly of centromeres in mitosis, this inversion may be recessively pure and lethal. Experiments in homologous gene mutants in human cells and zebrafish have shown that inactivation of CENPN will have serious adverse effects. In fact, observations of the tasseled sandpiper family have proven that this inversion is pure and lethal. Since the proportion of "satellite" fringed sandpipers in the population is greater than 5%, heterozygous fringed sandpipers containing "satellite" alleles must improve their survival rate by at least 5% to counteract the pure and lethal effects.
Küpper and colleagues at the University of Graz in Carl Froomzens, Austria, found that an important factor in improving survival rates is that both the "satellite" and "Fidel" fringed sandpipers have larger testicles and can produce more numerous and more motile sperm. In this way, even if their mating rate is not necessarily higher than that of the "independents", they can have a certain advantage in producing offspring.
There are two main reasons why dominant genes accumulate this lethal mutation, one of which is that the allelele is rarely purified, resulting in fewer options for eliminating such mutations. Second, in heterozygotes, recessively lethal mutations are difficult to opt for removal. There are also phenomena in other species where supergenes carry harmful mutations, such as the white-throated finch and the African white phoenix butterfly.
If known to be in danger of purity and death, would the female choose to avoid choosing a "satellite" male and save her offspring from threat? In other species, there are strong mate avoidance options. For example, in white-throated finches, white-striped individuals usually choose a brown striped mate, which results in a very rare number of pure and white-striped individuals with poor adaptability. This may be a feedback mechanism that reduces the emergence of pure and genotypes through non-random mating and further reduces the accumulation of harmful mutations. At present, non-random mating has not been found in tasseled sandpipers, and it is thought that after we have a clear understanding of the mechanism of action of super genes, it will be interesting to further observe their mating choices in the wild population.
03
Who is the hero of the "sister-in-law technique" differentiation?
In the animal kingdom, birds are typical of appearance societies, and many birds display beautiful feathers during the courtship season. In the supergene of fringed sandpiper, one of the candidate genes that play a role in coat color differentiation is the melanocorticin receptor 1 (MC1R) located inside the inverted region.
Lamichhaney and colleagues used genome-wide correlation analysis to discover four missense mutations in the gene of the "satellite," resulting in alterations in four amino acid residues that are conserved in both birds and mammals. There are also four wording mutations in this gene of "Fidel". Among them, a missense mutation shared by "satellite" and "Fidel" may be the cause of the coat color change. Because the same mutation in red-footed is also associated with lighter coat color. The researchers believe that in the "satellite" fringed sandpiper, the MC1R gene works together with other sex hormone genes to lead to the appearance of white feathers. The MC1R gene of the "satellite" must be a dominant gene, because the "satellite" fringed sandpiper is all heterozygote, and only the dominant gene can show traits. In addition, the MC1R mutant is specifically manifested in the feathers, because the coat color of females carrying the "satellite" allele and non-breeding "satellite" males is not significantly different from other individuals and does not exhibit the trait of light-colored feathers.
According to Küpper and colleagues, the unique appearance of the Fidel fringed sandpiper is more likely to stem from a mutation in phosphatidylinositol-4,5-diphosphate phosphodiesterase 2 (PLCG2), a gene that undergoes complex deletions and recombination after inversion, which may lead to complete inactivation of the protein. PLCG2 encodes a transmembrane signaling enzyme that interacts with the epidermal growth factor receptor EGFR associated with feather growth. Therefore, in fidel fringed sandpiper, the loss of secondary sex characteristics of feathers and behavior may be due to variation and inactivation of PLCG2.
Appearance is of course very important, but the action in "pampering sisters" is also indispensable. For behavioral changes, there are also candidate genes in the super genes. Three deletions occurred in the "satellite" and "Fidel" supergenes, located in HSD17B2 (steroid (17-β) dehydrogenase 2) and SDR42E1 (short-chain dehydrogenase/reductase family 42E, member 1), respectively. HSD17B2 and SDR42E1 are both important enzymes in sex hormone metabolism. HSD17B2 can catalyze the transformation of estrogen and androgens, including testosterone and dihydrotestosterone, into less active types. Two unique deletions and two unique repetitions were also found in the "Fidel" supergene, which may be related to the unique behavior of "Fidel". During reproduction, testosterone levels were higher in the "independent" circulatory system, while in the "satellite" and "fidel" circulatory systems and androdenediones were higher, reflecting the regulation of different behaviors by the hypothalamic-pituitary-gonadal system.
In nature, species with super genes like fringed sandpipers are not uncommon. This principle of controlling complex biodiversity in a simple and unambiguous way is a wonderful stroke in evolutionary biology. Phenomena similar to supergenes include inbred incompatibility in plants, partial separation in drosophila and mouse meiosis, and the most common sex chromosome. The study of the super genes in fringed sandpipers not only demystifies the fringed sandpiper's rich "sister-stirring" skills, but also provides us with valuable wealth for studying recombination and adaptive evolution.
Resources:
1.Jiggins C D. A flamboyant behavioral polymorphism is controlled by a lethal supergene[J]. Nature genetics, 2016, 48(1): 7-8.
2.Küpper C, Stocks M, Risse J E, et al. A supergene determines highly divergent male reproductive morphs in the ruff[J]. Nature genetics, 2015.
3.Lamichhaney S, Fan G, Widemo F, et al. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax)[J]. Nature genetics, 2016, 48(1): 84-88.
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