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Blind snakes slink, wriggle, and bump through the pages of The Anatomical Record in a novel Special Issue

2021; Wiley; Volume: 304; Issue: 10 Linguagem: Inglês

10.1002/ar.24728

1932-8494

Jeffrey T. Laitman, Scott C. Miller,

Animal and Plant Science Education

Poor snakes. Snakes have had a really bad reputation since, well, since almost forever. Indeed, the very first thing many of us learned in Bible Class as a child was the story of Adam and Eve in the Garden of Eden with that miserable snake. If not for that serpent, we would all still be enjoying the unrelenting pleasures of a bucolic world! Through time, snakes (serpents, as they were often called) have accrued a lot of bad press. Even The Lord God made it clear that snakes were to be outcasts forever, saying in Genesis 3:14: "The Lord God said to the serpent, Because you have done this, cursed are you above all livestock and above all beasts of the field; on your belly you shall go, and dust you shall eat all the days of your life." (KJV) It does not get any clearer then that; you snakes are definitely on the bad list! Indeed, snakes are mentioned some 80 times in The Bible and it is not to praise their shimmering scales. Interestingly, not all cultures despised snakes. For the ancient Greeks, for example, snakes could at times be sacred symbols and guardians of the underworld, or messengers between the upper and lower worlds, as they could go between cracks in the earth. The shedding of their skin represented to some longevity, and even immortality. Snakes also appear in the Rod of Asclepius, the Greek god of healing. Although having some positive supporters, the negative press of biblical history was just too overwhelming; no fuzzy snakes to buy for toddlers or nighttime stories about the three blind snakes! Indeed, even modern cult hero Indiana Jones suffered from ophidiophobia (fear of snakes; Ophidia is the biological clade that includes snakes and other squamates more closely related to snakes than to other reptiles) and he famously uttered in the iconic Raiders of the Lost Ark, "Snakes. Why did it have to be snakes?" (1981; as an aside, Indy failed to recognize that many legless lizards were actually used to fill that room). Indy would also definitely have found the skies most unfriendly had he been trapped in the 2006 thriller Snakes on a Plane, which gave those of us with some fear of flying even more of a reason to take Amtrak! Although we all like to peer at snakes through the safety of thick glass in "The Snake House" at our local zoo, most of us (it is estimated that one-third of all humans are ophidiophobic) prefer to keep our distance. Not so, the herpetologists, serpentologists, zoologists, paleontologists, and comparative anatomists who have explored the anatomy, biology, and evolution of the group of snakes collectively known as "blind" snakes. Falling in the Families Typhlopidae, Gerrhopilidae, Leptophlopidae, Xenotyphlopidae, and Anomalepididae, this remarkable group contains over 450 species with most being typhlopids and leptotyphlopids (typhlopids are often called "blind" snakes and leptotyphlopids "thread" snakes; you have to have a sharp eye to see who is who in this world!) Blind snakes are the smallest of all snakes, some so diminutive that they are often confused with earthworms by the non-cognoscenti (what ignominy being confused with a lowly invertebrate!) This month's Special Issue, "Blind Snakes," Guest Edited by Rebecca Laver from the Research School of Biology at the Australian National University in Canberra and Juan Daza from the Department of Biological Sciences at Sam Houston University in Texas, shines a bright light, and focused vision, that explores the world of these extraordinary subterranean sleuths. This issue was organized, in part, to honor the accomplishments of noted herpetologist Richard Thomas and the seminal findings he has had in the field (Laver & Daza, 2021, this issue). Those spearheading this issue, Laver and Daza, are two dynamic superstars in the slithering field of squamates and have already individually published many studies on the anatomy, ecology, and evolution of all sorts of lizards, geckos, and their relatives. Indeed, Daza is an Anatomical Record regular, having Guest Edited a wonderful Special Issue of our journal, "New Advances in Morphology and Evolution of Living and Extinct Squamates" in 2014 (Albertine & Miller, 2014; Daza, 2014) as well as frequently publishing with us on lizards and their ilk (e.g., Daza & Bauer, 2010; Daza, Bauer, & Snively, 2014; Holovacs, Daza, Guerra, Stanley, & Montero, 2020). Daza's co-guest editor Laver, although new to our journal, has similarly studied a range of squamates from little geckos (e.g., Laver, Nielsen, Rosauer, & Oliver, 2017) to immense Komodo dragons from Indonesia (Laver et al., 2012). (Neither of the authors of this editorial will ever get to within munching distance to these 10 ft. long apex predators that occasionally eat humans!) This special issue was overseen by editorial co-author Scott Miller (SM) of the University of Utah in his role as associate editor of The Anatomical Record. JL would like to note the following regarding SM, so Scott, turn away for a second. SM is among the most interesting people in the history of our Anatomical Record family. Yes, he is an internationally respected bone biologist and one fine musician. But he is a lot more, much of which we do not really know about. For example, SM has long been funded by the U.S. Department of Energy, and for those who do not know much about that group they are not in charge of light bulbs and windmills. Much of their activity has to do with secret nuclear stuff that I do not want to know about. When President of the American Association for Anatomy (the parent body of The Anatomical Record) I was requested by the Anatomical Society of Kazakhstan to please send a noted anatomist to help them form, and promote, their society (the AAA President gets lots of interesting requests). In reviewing my list of possible candidates, there was one whose background file noted frequent visits to the region of central Asia and contiguous Eastern Europe, and who was also a "Gold" Level flyer on Aeroflot (the Russian state Airline). Guess who? I leave it to you to fill in the blanks of who/what he was visiting in these regions (by the way, his laboratory in Utah has Geiger Counters). SM was accordingly tapped, and was so successful in his mission that I get yearly "thank you" notes from the Kazakhstanis with pictures of their horses! I think that there is a statue of SM somewhere in Almaty (the capital). (By the way, some Kazakhstanis subsequently joined the AAA and even came to our meetings!) This special Special Issue has thus been lovingly shepherded by two squamate dynamos and one really interesting "whatever-he-is." While they have collectively put together a most novel collection of manuscripts on blind snakes and their relatives, our journal has had snakes slither through our pages for some time. They have been studied in a variety of ways and for purposes ranging from zoological examinations to understand species differences, as vehicles to explore aspects of reptilian evolution, and, particularly, as sources to understand the development of vertebrate anatomical and physiological systems. The first snakes to appear in The Anatomical Record can be found in a report by Yale researcher Henry Laurens in 1913 (Laurens, 1913) examining the atrio-ventricular connection in reptiles. While the majority of his specimens were assorted lizards and turtles, the shy, non-venomous, brown snake, Storeria dekayi, makes his list and so is our inaugural snake! While Laurens continued his work on the reptilian heart in The Anatomical Record (Laurens, 1915) snakes slide out of his reportage. They did, however, reappear in their own right in the study by Kunkel on the paraphysis and pineal region of garter snakes (1915), making this the first study starring snakes in our journal. Snakes made guest appearances in many ensuing studies (most of the light being on the attention-grabbing lizards!) but frequently also took center stage. Notable among these: De Renyi's study of kidney cells in the garter snake (1936); Thomas' comparative examination of the snake pancreas (1942); Bragdon's (1953) fascinating examination of the water snake's visceral endocrine organs in reference to its ventral scutellation (did you know what scutellation is? It is the arrangement/placement of scales—keep that handy for Jeopardy!); Fox's study on the comparative anatomy of the seminal receptacles of snakes (1956); Proske's study of nerve endings in the skin of the Australian black snake (1969); Jackson and Sharaway's study of lipid and cholesterol clefts in the lacunar cells of snake skin (1978); Jacobs and Sis's degeneration study of the dorsal column in garter snakes (1980); Rhoten's (1984) study on immunocytochemical localization of hormones in the garter snake pancreas; and Robinson's (1987) study of twitch and tonic fibers in snake muscle myofibers, these collectively giving some examples of our first eight decades with snakes. During this period, some giants in our field published on snakes in The Anatomical Record, and with apologies to other outstanding slithero-philes, we will highlight two. The first is one of the great comparative anatomists of the 20th century, Howard Edward Evans of the New York State College of Veterinary Medicine at Cornell University. "Howie" Evans, to the many that knew, learned from, and adored him, was a mainstay in the teaching and research of organismal and comparative biology at Cornell for over 50 years, starting on the faculty there in 1950. Evans had an enormous influence on generations of Cornelians. For example, one of JL's most accomplished graduate students, Joy Reidenberg, now a leading expert on all things whale (and who is always trying to push poor JL into the seas to get close to her friends) was an undergraduate disciple of Evans. Indeed, for her graduate school application, she sent an 8 x 10 photo of herself standing next to a half-dissected cow from Evans' dissection course (it worked; she was chosen immediately, funded, and subsequently has swum off into numerous publications in The Anatomical Record, for example, Reidenberg, 2007; Reidenberg & Laitman, 2008; Damien et al., 2019; see also Laitman & Albertine, 2019). Evans was a "Renaissance" anatomist and taught about, and published on, many species, occasionally in our journal (e.g., Evans, 1959; Watson, De Lahunta, & Evans, 1986). Early in his career, in 1955 (Evans, 1955), he published his first article with us on·wait for it—the osteology of Typhlops jamaicensis, our Blind snake (which Evans referred to with its degrading synonym, "worm" snake; we forgive him). Thus, Professor Evans is arguably the first to bring our burrowing heroes to The Anatomical Record! The second notable whose snakes crawled into our pages is Aron A. Moscona. Moscona was a long-time professor of Molecular Genetics and Cell Biology and of Pathology of the University of Chicago (1958–1992; to 2002 as emeritus), and was known to most of us not as a "snake" investigator but rather as a renowned developmental biologist and one of the pioneers in uncovering how cells "recognize" each other and arrange themselves to form tissues and organs of the body. Moscona was internationally revered for his groundbreaking work, and was elected a member of many esteemed bodies including the National Academy of Sciences and the American Academy of Arts and Sciences. Simply put, Moscona was one intellectual heavyweight. Interestingly, his early love was not developmental biology but, you guessed it, snakes, particularly their pancreas. Early in his career (he was Israeli, his PhD was in endocrinology-biochemistry from the University of Haifa, and in 1953, joined the faculty of the University of Jerusalem), he explored the region in snakes, resulting in his early publications being on them (e.g., Moscona, 1954). Toward the twilight of his career, Professor Moscona returned to his fascination with snakes. Indeed, his next to last publication was on the pancreas in snakes, including blind snakes, and appeared in The Anatomical Record (Moscona, 1990). Were it not for the strong hand and swift kicks by then Editor-in-Chief of The Anatomical Record, A. J. (John) Ladman (who steered our journal for 30 years, 1968–1998) Professor Moscona's beautiful manuscript may have been his last publication, or may not have happened at all. The reason for this was a problematic reviewer and new member of the Editorial Board who was giving the august professor all sorts' grief. This editor was JL, who in his desire to have every "i" dotted and "t" crossed was insisting on having complete documentation on the exact methods of euthanasia employed down to doses and timing for each snake used in the study. Poor Professor Moscona, a true gentleman and scholar, kept explaining that most snakes were from collections at the Hebrew University that were given to him over the years for dissection and study. JL pressed on and on…until the hand of God (or John Ladman, who was a close second) figuratively landed on his head! Johnny Ladman (who was built like a wrestler and was one tough New York City kid) called JL and made it clear during a one-sided telephone call ("Jeffrey, you are NOT to speak. Got it?" said Ladman; "Yes" said JL; "Quiet! You're speaking!") that if the science was solid and the data clear that JL should move, NOW! (The monologue was a bit more colorful—Ladman was a NYC street kid after all—but not for dissemination in our scholarly journal). And JL did as instructed. The end result was the beautiful (Moscona did his own pen and ink drawings) and most valuable contribution on the snake pancreas, its anatomy, function, and evolution that appeared in our journal. Beginning in the 1990s, The Anatomical Record saw a wave of snake manuscripts slither onto our pages. This was due to a variety of factors, two most prominent: (a) More and more researchers were using snakes as base-line vertebrates to better understand the evolution of biological systems; (b) JL no longer was allowed to see snake manuscripts (this is why SM has overseen our previous issue on squamates and this current one). Some examples include: Amemiya and colleagues' studies on the crotaline snake pit receptors (Amemiya et al., 1999; Amemiya, Ushiki, Goris, Atobe, & Kusunoki, 1996); Young, Marsit, and Meltzer (1999) comparative study of the cloacal scent gland in snakes; Nakano and colleagues' study of the ultrastructure on snake infrared sensory organs (Nakano et al., 2000); Alibardi and Toni's (2005) study on the characterization of cornification proteins in the epidermis of snakes; Hofstadler-Dieques, Walter, Mierlo, and Ruduit (2005)'s creative three-dimensional reconstruction of the snake chondrocranium from histological sections; the very insightful study by Fourneaux et al. (2010) examining the evolution of rudimentary eyes in various squamate reptiles including, of course, Typhlops, the blind snake; Liu and colleagues' examination of the anatomy of snake venom via a proteomics approach (Liu et al., 2010); an examination on the ultrastructure of the sea snake kidney by Sever, Rheubert, Gautreaux, Hill, and Freeborn (2012); modeling the snake esophagus to understand its function and development by Cundall et al. (2014); Johnston's study on the homology of jaw musculature in snakes and lizards Johnston (2014); a most fascinating, and beautifully illustrated, study exploring the influence of sexual selection on the appearance of hemipenes (male copulatory organs) in Old World snakes (who knew?) by Andonov, Natchev, Kornilev, and Tzankov (2017); Trivino and colleagues' description of the first natural endocranial cast of a fossil snake from the Cretaceous of Patagonia (Trivino, Albino, Dozo, & Williams, 2018); Bassi, de Oliviera, Braz, and de Almeida Santos (2018)'s study on the anatomy underlying oocyte uptake in the coral snake; and Hall and colleagues' insightful study of bony tumors in snakes (Hall, Jacobs, & Smith, 2020). And that is just some of the snakes that have slid into the pages of The Anatomical Record! As can be seen by our brief review, The Anatomical Record has been "dancing with snakes" almost since the journal's birth. This Special Issue highlighting blind snakes and their close kin have made us smile (as well as learn!) as it is somewhat of a "feel good" story with the little guys taking center stage. No massive anacondas or nasty pit vipers hogging the limelight, our mighty little fossorial warriors have made it to prime time. This Special Issue is also in the best traditions of our journal that has sought to bring creative and novel, even if somewhat out of the limelight, science to our large audience. We thank our Editor-in-Chief, Heather Smith, and our former EIC, Kurt Albertine, for being strong supporters of always advancing the best of all science no matter how focused, or how narrow a lane, the research might appear. So, we hope that you, like us, will enjoy learning about the mighty little blind snake, and remember, do not call them worms!