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Adaptive Introgression across Species Boundaries in Heliconius Butterflies

Smithsonian Libraries
It is widely documented that hybridisation occurs between many closely related species, but the importance of introgression in adaptive evolution remains unclear, especially in animals. Here, we have examined the role of introgressive hybridisation in transferring adaptations between mimetic Heliconius butterflies, taking advantage of the recent identification of a gene regulating red wing patterns in this genus. By sequencing regions both linked and unlinked to the red colour locus, we found a region that displays an almost perfect genotype by phenotype association across four species, H. melpomene, H. cydno, H. timareta, and H. heurippa. This particular segment is located 70 kb downstream of the red colour specification gene optix, and coalescent analysis indicates repeated introgression of adaptive alleles from H. melpomene into the H. cydno species clade. Our analytical methods complement recent genome scale data for the same region and suggest adaptive introgression has a crucial role in generating adaptive wing colour diversity in this group of butterflies.

Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies

Smithsonian Libraries
Homoploid hybrid speciation is the formation of a new hybrid species without change in chromosome number. So far, there has been a lack of direct molecular evidence for hybridization generating novel traits directly involved in animal speciation. Heliconius butterflies exhibit bright aposematic color patterns that also act as cues in assortative mating. Heliconius heurippa has been proposed as a hybrid species, and its color pattern can be recreated by introgression of the H. m. melpomene red band into the genetic background of the yellow banded H. cydno cordula. This hybrid color pattern is also involved in mate choice and leads to reproductive isolation between H. heurippa and its close relatives. Here, we provide molecular evidence for adaptive introgression by sequencing genes across the Heliconius red band locus and comparing them to unlinked wing patterning genes in H. melpomene, H. cydno, and H. heurippa. 670 SNPs distributed among 29 unlinked coding genes (25,847bp) showed H. heurippa was related to H. c. cordula or the three species were intermixed. In contrast, among 344 SNPs distributed among 13 genes in the red band region (18,629bp), most showed H. heurippa related with H. c. cordula, but a block of around 6,5kb located in the 39 of a putative kinesin gene grouped H. heurippa with H. m. melpomene, supporting the hybrid introgression hypothesis. Genealogical reconstruction showed that this introgression occurred after divergence of the parental species, perhaps around 0.43Mya. Expression of the kinesin gene is spatially restricted to the distal region of the forewing, suggesting a mechanism for pattern regulation. This gene therefore constitutes the first molecular evidence for adaptive introgression during hybrid speciation and is the first clear candidate for a Heliconius wing patterning locus.

Genomic Hotspots for Adaptation: The Population Genetics of Mullerian Mimicry in the Heliconius melpomene Clade

Smithsonian Libraries
Wing patterning in Heliconius butterflies is a longstanding example of both Mullerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are "hotspots" for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in Heliconius melpomene and relatives. Alleles at HmB control the presence or absence of the red forewing band, while alleles at HmYb control the yellow hindwing bar. Across HmYb two regions, separated by similar to 100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at HmB a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both HmYb and HmB there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the HmB locus, the kinesin shows differences in wing disc expression between races that are replicated in the co-mimic, Heliconius erato, providing striking evidence for parallel changes in gene expression between Mullerian co-mimics. Wing patterning loci in Heliconius melpomene therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years.

Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

Smithsonian Libraries
The evolutionary importance of hybridization and introgression has long been debated(1). Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation(2-5). We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.

Before the 'Baby Shark' Song Made the Hot 100, 'Silly Symphonies' Were All the Rage

Smithsonian Magazine

Thank a South Korean educational content brand for producing, if not the definitive, assuredly the most-listened-to, version of the earworm “Baby Shark,” the children’s song chomping its way through its second week on the Billboard Hot 100 Chart.

You may have encountered an earlier variation of the song—and its accompanying dance moves—back in summer camp (or, like this writer, inexplicably during a middle-school unit on marine life). It was a little over a decade ago, though, in 2007, when “Baby Shark” teased its true potential when a video of the song went viral in Germany.

That turned out to be small potatoes compared to the Pinkfong remix. The brand behind the sensation has produced tens of thousands of children’s videos, including multiple variations on “Baby Shark.” But one of these versions went supernova after it was published to YouTube in 2016. In it, the Seoul-based company laid a K-pop beat underneath the vocals and plucked two cherub-cheeked children to do the hand motions of the lyrics for the video, which also features animations of candy-colored, decidedly heteronormative sea creatures and Pinkfong’s own magenta fox, kitted up in snorkel gear for the occasion.

The video has been the subject of a very-21st century regurgitation cycle ever since. With 2.1 billion views to its name and counting, at this point, its debut on the Billboard chart—with thanks to Billboard’s decision to incorporate YouTube data into its mysterious music-selection algorithm back in 2013—feels more like a formality than anything.

If you haven’t heard the song that the New York Times calls “as infectious as anthrax,” it’s loosely centered around three generations of hungry sharks (Doo Doo Doo Doo Doo Doo). That’s pretty much it. In some versions, the sharks eat you. In the Pinkfong version, the adorable children make it out safe, and that’s “the end (Doo Doo Doo Doo Doo Doo)/ the end (Doo Doo Doo Doo Doo Doo).”

Around the time Pinkfong’s “Baby Shark” mania had the Ellen Degenereses and James Cordens of the world subjecting us to the #babysharkchallenge, Bob Cunningham, an educator and senior adviser for the nonprofit consortium Understood.org, attempted to pin down just what made the Pinkfong song so very listenable. The formula he describes to the Associated Press—a “catchy rhythm,” “silly sounds,” and “colorful and cute animation”—is reminiscent of what gave rise to the first iteration of children’s hits.

Children’s music has been part of the music industry since the get-go. “Ever since there has been a music business, there has been a children’s music business,” explains Simon Frith, a professor of music, in his collection of essays Taking Pop Music Seriously. Just 11 years after Thomas Edison debuted the phonograph in 1877, an unknown employee of the Edison company recorded "Twinkle, Twinkle Little Star” for the company’s short-lived talking doll venture. When that recording was found in the desk of an assistant in the 1960s, it earned the nursery rhyme the distinction of being the earliest-known children’s recording, the earliest-known commercial recording, and perhaps even “the first recording to be made by someone who was paid to perform for a sound recording,” according to the Library of Congress.

Edison’s phonograph was, undeniably, a game changer for the music industry. Suddenly, music was portable, affordable and repeatable, writes Mark Katz, a scholar on music and technology in the journal American Music. Music teachers, in turn, believed the phonograph would keep American youngsters away “from the temptations of popular music” by exposing them to what they considered “good” music. "If the children enjoy Schumann's “Trdumerei,” Schubert's “Serenade,” and the “Pilgrim's Chorus” from [Wagner’s] Tannhauser," argued one music teacher in 1911, "they will not care to hear rag-time and cheap street music."

That… didn’t turn out to be quite the case. “Baby Shark” stands in the shoes of Walt Disney's Silly Symphonies, which also matched music to animation to great success using, wait for it, catchy rhythms, silly sounds, colorful (when the technology allowed), and sometimes cute, always eye-catching, animation.

Unlike “Baby Shark,” this “musical novelty” series of short films released from 1929 to 1939 achieved critical success in addition to popular success (seven of the shorts won the Academy Award for Best Animated Short Film). The Sillies did so by marrying clever animation with a range of music “encompassing classical melodies, traditional folk tunes, operatic themes—and popular songs,” film scholar J.B. Kaufman explains in Animation World Magazine, a genre that birthed a host of imitators, notably work by rivals at Warner Bros.

Silly Symphonies came just at the right moment. In the 1920s and ’30s, composers and graphic artists were exploring the frontiers of animation. “What all these experimenters shared was a common interest in, indeed a fascination for” finding the “rhythm” between sight and sound on screen, writes music scholar Jon Newsom in the Quarterly Journal of the Library of Congress.

That balancing act was such a big deal at Disney HQ that the studio’s exacting synchronization of music and animated movement began to be referred to within the industry as “mickey mousing.”

Theater organist and orchestra leader Carl W. Stalling was a big part of how that came to be, engineering a way to allow his musicians to hear what was happening in an animated sequence through an ingenious “click track.” Stalling was also the one who convinced Disney to let him score the Sillys before they were animated, beginning with the very first mini-musical, “The Skeleton Dance” (1929).

A regular on the list of all-time best animated shorts, the inaugural Silly featured a spooky night full of owls, black cats and full moons. The cartoon was also put together around Stalling’s score, which Disney agreed would “take precedence,” writes Tighe E. Zimmers, a researcher on popular song composers.

The alchemy of the music inspiring the animation was groundbreaking. Not so unlike the Pinkfong “Baby Shark” song, which pulls its opening bars from the Jaws theme, and leans into K-pop dance inspiration, Stalling famously used whatever music he thought fit the bill for his work.

He “would draw on his training, ransacking the entire literature of classical and popular music to weave a suggestive undercurrent to the screen action,” Tebbel writes, something he did most famously in his later career scoring the Merrie Melodies shorts produced by Warner Bros., but also employed in the Sillies, which included a rich musical lexicon of excerpts that ranged from “Moonlight Sonata” to “Row, Row, Row Your Boat.” (Cartoonresearch.com has the exhaustive list of sounds that appear in the Sillies, and it’s impressive.)

The true “going viral” moment for Sillies came with the debut of “The Three Little Pigs” at New York’s Radio City Music Hall on May 27, 1933.

“It received a sensational public response as it was shown in neighborhood theaters, becoming the most phenomenal short cartoon of its time,” writes classic cartoon researcher Devon Baxter.

Disney had imagined the cartoon as a light, humorous operetta, explains Baxter, and the dialogue was sung in rhythm by the anthropomorphized pigs, who bob and sway hypnotically as they work against their foil, the Big Bad Wolf. The cheery cartoon is immensely watchable, and for Americans weathering the Great Depression, its happy-go-lucky tone was just what children—and adults—needed.

Songwriter Ann Ronell of Tin Pan Alley fame, with whom Disney had previously collaborated, worked with composer Frank Churchill on “Who’s Afraid of the Big Bad Wolf,” (who did what for the song remains under debate), and their result was pieced together throughout the cartoon.

Sol Bourne, general manager of Irving Berlin Music, Inc., believed he had a massive hit on his hands when he heard the song on screen. “Bourne knew an individual song, tied in with a movie or a cartoon, created synergy and helped sell both entities,” Zimmers writes. Subsequently, Irving Berlin Music negotiated to get Disney Studio’s music rights.

The partnership was unprecedented. In a 1963 correspondence cited in Zimmers’ biography on Ronell, the songwriter explained that “cartoon background music wasn’t taken seriously in those days and no song had ever been published previously from the cartoon film industry.” But Bourne was right; an audience was waiting.

Like “Baby Shark” moving from YouTube to a chart debut, “Who’s Afraid of the Big Bad Wolf?” made a definitive statement on its own. TIME magazine declared it was one of the year’s “catchiest songs," and more than 201,000 copies of sheet music for it was sold in the second half of 1933 alone.

Before 1934 had even begun, Kaufman and film and media scholar Russell Merritt write in their Silly Symphonies companion book, “the song had been widely recorded and had set a new precedent by introducing the Disney studio into the world of popular music,” and—who knows— possibly even threw the chum in the water for what was lurking deep below, a catchy family of sharks (Doo Doo Doo Doo Doo Doo).