Elaina Tuttle didn’t set out to discover the first avian “supergene.” But she did just that while studying White-throated Sparrows for 27 years in New York’s Adirondack Mountains.
By Rex Graham
The scenic area is home to more than 100 species of songbirds, raptors and waterfowl. The attractive White-throated Sparrow seems to be a typical songbird rather than genetically unique among all species in the animal kingdom.
White-throated Sparrow – something amiss
There are only hints that something is amiss: brightly colored white-morph sparrows almost always pair with more drably colored tan morphs. Birdwatchers might assume that the brightly colored white morphs are males, and the tans are females. In field guides there are no gender icons next to white and tan morphs because either morph can be male or female.
For the majority of bird species that exhibit “sexual dichromatism,” males and females look different. In many sparrow species, especially those most closely related to White-throated Sparrows, the sexes look alike. Typically, males are slightly larger.
Color morph mysteries
Males and females of each color morph exhibit subtle plumage and size differences. White-throated Sparrows exhibit behavioral dichromatism: white-morph males and females are more aggressive than the tan morphs. Of course, males mate with females, but the more aggressive whites, almost always mate with the less aggressive tans.
Sparrow with ‘4 sexes’
“The species operates as though there are 4 sexes,” Tuttle, the late biology professor at Indiana State University said in a paper published in 2016 in Current Biology.
The genetics of the 4-sex species that Tuttle described would have given Charles Darwin and Gregor Mendel headaches. Underlying the bizarre inheritance is a system in which multiple behavioral traits and crown-stripe color are inherited as if they are part of one supergene.
Tuttle and her students and colleagues documented a variety of behaviors attached to the White-throated Sparrow supergene:
- White morph males and females sing more than tans.
- White males defend their territories more aggressively than tan males, but guard their tan mates less forcefully than tan males defend their white females.
- White males trespass onto other White-throated Sparrow territories much more than tan males.
- White females perform more courtship displays seeking copulation more that tan females.
- White males are more promiscuous than tan males and are more likely to mate with females outside their pair bonds than tan males.
- White females and males provided less parental care than tan females and males.
- White females accept greater risks that a neighboring female will sneak in and lay an egg in her nest than tan females.
This tight linkage of so many of behaviors with crown-stripe color is not an example of Mendelian genetics. Mendel famously showed that genes for peapod color and shape are inherited independently. Independent assortment of traits also held for seed color and shape, and plant height.
This independent assortment of genes and their outward expression as phenotypes is a bedrock principle of genetics. In the process of formation of egg and sperm (or pollen), only 1 chromosome of each pair in a genome goes into the gamete. In this process, called meiosis, each pair of chromosomes shuffle all their genes like two decks of cards at a gambling casino. In this process of recombination, independent assortment of genes is guaranteed.
Why doesn’t recombination work on the sparrow’s supergene? The phenotypes Tuttle and her colleagues so carefully documented always stick together as a unit and the two decks of cards aren’t shuffled together.
Tuttle and geneticists at Emory University in Atlanta, Georgia, discovered how non-Mendelian inheritance works in the White-throated Sparrow. A 1,000-gene cluster (the supergene) on the bird’s chromosome 2 is inherited in each chick as if it were one Mendelian gene, the supergene.
The white and tan morphs have virtually all the same genes on each of their chromosome 2s. However, the order of the genes is slightly different in each, which makes a huge difference. (Different versions or alleles of the 1,000-plus genes on chromosome 2 are present on chromosome 2 of the white and tan-morphs.)
Supergene’s inversion genesis
Based on genomic studies of the white and tan morphs, scientists have come up with the reason why the 1,000 genes in the supergene on chromosome 2 aren’t randomly shuffled via recombination.
- The tan’s supergene has the default linear (let’s say alphabetical) gene order:
A-B-C-D-E-F-G-H-I-J-K-L-M-N-O-P-Q-R-S-T-U-V-W-X-Y-Z (tan morph)
- However, in what scientists think was a 2-step process, a huge section (in parenthesis) of chromosome 2 temporarily inverted from the ancestral . . .
Into an end-to-end inversion:
- A second inversion reverts almost all of the first flip, but fewer parts (in parenthesis) are included in the second inversion:
- The final result is the chromosome 2 supergene carried by the white morph:
A-X-W-C-D-E-F-G-H-I-J-K-L-M-N-O-P-Q-R-S-T-U-V-B-Y-Z (white morph)
A-B-C-D-E-F-G-H-I-J-K-L-M-N-O-P-Q-R-S-T-U-V-W-X-Y-Z (tan morph)
Most of the genes don’t line up, which severely limits recombination.
The geneticists said this double-inversion process may have occurred 2.2 million years ago. It would have become a non-recombining supergene because the genes on the white morph and tan morph’s second chromosome have shifted relative to each other. Since white morphs (almost) always mate with tan morphs, they are heterozygous for the supergene.
As a result of the misalignment of tan and white chromosome 2s, the usual card shuffling of genetic recombination that normally occurs between pairs of homologous pairs of chromosomes during meiosis doesn’t take place. When a rare recombination occurs, the result would be inviable gametes or embryos with extra or missing genes, according to Indiana University Biology Professor Loren Rieseberg.
Other closely related songbirds don’t have supergenes, so how did the White-throated Sparrow originally acquire one? Nobody knows.
It could have acquired it by hybridizing with another species that carried a supergene. “The donor species may be extinct,” Tuttle said in the Current Biology paper co-authored by scientists at Indiana State, Stanford University, East Carolina University, Washington University in St. Louis, Missouri, and the University of Illinois in Urbana-Champaign. Another option is that the sparrow’s supergene simply arose spontaneously by the double-inversion process.
Over 2.2 million years of no recombination, lethal and deleterious recessive mutations have undoubtedly cropped up in the supergene. White-tan matings yield offspring that would be heterozygous for those mutations. Only white-white or tan-tan pairs could produce chicks with bad homozygous-recessive gene combinations.
Indeed, Tuttle reported that only 3 of 1,989 birds tested were homozygous for the white-white supergene. In these rare cases, both chromosome 2s would align correctly and recombination could occur. This process could, in theory, help to remove deleterious mutant genes.
However, Tuttle noted that since white morph males and females both have poor parenting skills, any of their surviving chicks would be more likely to starve or be eaten by predators. Indeed, the offspring of two white-morph parents were found to grow significantly more slowly than chicks from white-tan pairs.
Tan-tan combinations could, in theory, make better parents. But that combination has not yet been detected by Tuttle’s team over years of genetic analysis of thousands of captured birds. It’s possible that tan morphs have more lethal recessive alleles: homozygous tan-tan embryos would either not develop or die before hatching.
Modern genomic analyses are credited with helping to discover 3 supergenes in the Ruff, a Eurasian sandpiper. Male Ruffs exhibit any of 3 male mating morphs, each with a signature body size, ornamentation and plumage, and aggressive mating mode.
Supergenes also have been found in flower morphs of some plants, shell morphology variants in some snail species, and some butterflies with multiple wing-pattern morphologies designed to mimic unrelated poisonous butterflies that predators avoid.
Scientists have also found that the “t complex” on chromosome 17 of the House Mouse is a supergene.
“The t complex is composed of a set of adjacent inversions that are hypothesized to have been sequentially added to the complex as a mechanism to recruit new alleles and increase the fitness of that supergene,” the Emory University scientists said in the journal Genetics. “Chromosomal inversions, therefore, have unique and established genetic characteristics that can have a profound influence on the evolutionary process.”
Unlike the mouse, Tuttle, Rieseberg and others think that most supergenes may be too costly, too prone to degradation, or both to persist indefinitely or to expand. In White-throated Sparrows, Tuttle thought simple logistical problems also reduce the probability that the species and/or its supergene will persist.
“In part, this instability arises because 4-sex systems have a 2-fold increase in some aspects of reproductive effort, such as finding a mate,” Tuttle said. “If such 4-sex systems are truly unstable, the persistence of the inversion-based plumage morph polymorphism found in the White-throated Sparrow may be transient.”
EDITORIAL NOTE: Elaina Tuttle, 52, died June 15, 2016, at a hospital in Indianapolis, Indiana. She published many scientific papers based on her studies of White-throated Sparrows in New York and Fairy Wrens in Australia. She was associate editor of The Auk.