The Guatemalan beaded lizard and its complete genome

Zoo Atlanta is renowned for our conservation breeding program for what is arguably the most endangered lizard species in the world, the Guatemalan beaded lizard (Heloderma charlesbogerti). This species was discovered for science by my former graduate advisor, Dr. Jonathan A. Campbell, after hearing about it from local villagers in an obscure desert valley in eastern Guatemala known as the Motagua Valley. Finally, he secured a sample in the mid-1980s and a few more over the next few years. Those animals served as the basis for the formal taxonomic description and, after living in comfort at the facilities of his institution, the University of Texas at Arlington, he decided the lizards would be better served being at Zoo Atlanta. Our ongoing breeding program was launched based on those founder animals in 2000.

Initially, breeding them was a surprising challenge, but eventually our Herpetology Department learned their secrets, and now the colony has grown to the limits of facility can accommodate. A number of those animals will be transferred to the national zoo in Guatemala, La Aurora Zoo, later in 2023, when the multiple layers of paperwork are complete. There, they will hopefully reproduce and their offspring will be released into a fully protected reserve bearing their name, Reserva Heloderma. The reserve, by the way, is open to ecotourists and is a wonderful and fascinating place to visit and be guided around by truly knowledgable local naturalists (https://www.instagram.com/reservanaturalheloderma/). I’d suggest visiting in the mid-summer rainy season, when animals are more active and the vegetation is green.

Besides establishing the breeding colony, we have also conducted a number of studies on the basic biology of this incredibly reclusive species. They are difficult enough to simply encounter in the wild, so determining their ecology and behavior is very challenging and, for some question, impossible. For example, our studies have revealed the details of their reproductive biology, such as windows of fertility and normal clutch size, as well as the somewhat unusual fact that females cannot store sperm across multiple years, as can many other lizard species. We also now know, based on genetic screening of the offspring, that both males and females are promiscuous. In other words, during the breeding season both sexes mate repeatedly with different individuals. That would be very difficult to observe directly because the animals are so shy, but the genetic signatures clearly showed this to be the case. A single clutch of eggs may have perhaps three or four fathers, and each of those fathers may have mated with multiple females. This is an interesting aspect of their biology, to be sure, but also crucially important in managing a conservation breeding colony so as to avoid accidentally inbreeding the population. We have learned Guatemalan beaded lizards are not nearly as adept cognitively as are monitor lizards in learning and remembering puzzle-based tasks. This is a fascinating insight into how fundamentally different are these two types of lizards. Not all lizards think equally, as it turns out!

Joining forces with our geneticist colleagues at Georgia Tech, we decided to decipher the sequence of the entire genome of this species. You may recall a few years ago when we very proudly announced the entire genome of the Komodo dragon (Varanus komodoensis; https://zooatlanta.org/genome-of-the-dragon/). Of the many thousands of species of lizards, we know the complete genome of only about eight of them. Zoo Atlanta can be very proud to say that we have now partnered with geneticists to unravel the genome of two of these eight lizard species. Reconstructing a genome is quite challenging, even if the sampling is quite easy—a drop of blood obtained from the blood sample drawn by the veterinarians as part of their routine health monitoring. Aside from geneticists (Dr. Mike Goodisman, Dr. Carl Dyson, Dr. Aaron Pfennig, and Dr. Joe Lachance) the team included Guatemalan ecologist and the world’s expert on these lizards, Dr. Daniel Ariano-Sánchez from Universidad del Valle in Guatemala City, and myself. Dr. Ariano and I are not geneticists to the same degree that our brilliant genetics collaborators are not herpetologists. Altogether, this was a great team that brought a holistic perspective on the lizard.

Why are genomes such a big deal? Arguably one of the biggest scientific breakthroughs of the 20th century was the announcement of the complete human genome. The ability to understand the genetic basis for essentially everything that happens in a human body is coded in that DNA sequence. Every time your doctor advises you on matters such as heritable diseases, such as Huntington’s disease, certain cancers, Alzheimer’s disease, etc., you can thank the Human Genome Project. The initiative to understand the human genome was driven largely by the enormous value it would bring to human health. Our previous work with the Komodo dragon was driven largely by questions related to its unusual metabolism and circulatory system that acts more like a mammal than a reptile. This beaded lizard work was driven by conservation concerns regarding the ancient and recent history of the wild populations. Regardless of the interests and intents of the original team that assembles the genome sequence, the entire dataset is made publicly available so that any team anywhere in the world can use it to inform their specific questions. The legacy of the individual beaded lizard we sampled will survive for perpetuity. That remarkable individual, shown here, was one of the original individuals that Dr. Campbell encountered in 1984. This male was a large adult individual at that time, and lived another 38 years mostly at Zoo Atlanta. We estimate that the animal was approximately 50 to 60 years old when it passed away from natural causes in 2020. So, we now know that this species can live to be at least 50 years of age.

The analytical details are quite mind-boggling and I will skip them here, but believe it or not, one can infer loads of information about the history of population fluctuations in an entire species from the complete genome of a single animal. Given the grave conservation status of this species, this was important information to help us put their current plight into a historical perspective. What we found was fascinating.

Using all available historical data and the goldmine that is our genome sequence, we determined that this species likely originated on the far western, Pacific coastal region of the country. All of its closest relatives, three beaded lizard species in Mexico and the gila monster in northwestern Mexico and southwestern USA, are distributed generally along a geographic line that parallels the Pacific coast, so the presence of the Guatemalan population on the far eastern side of the landmass, associated with the Atlantic Ocean, seems odd with regards to this pattern. We believe that the species originated near the Pacific and dispersed afterwards across the country to its current environs in the eastern Motagua Valley.

The genome tells us that the species, regardless of its geographic location, suffered a massive decline in population size about 400,000 years ago, stabilized again around 200,000 years ago, dwindled again around 60,000 years ago, and reduced again about 10,000 years ago. The problem with our cross-country dispersal hypothesis is that the massive Atitlan Volcano, and others that form a very steep line of volcanoes along the Pacific coast of Guatemala, would make it impossible for these lizards to cross that barrier. But the geological record tells us that an area, appropriately known as the Amatitlan Cauldron, experienced severe landscape-scouring volcanic activity around 300,000 years ago. While subsequent volcanic activity has formed the currently unsurpassable geographic barrier, that initial volcanism was cataclysmic, likely being partly responsible both for the historical steep populational declines we documented in the genome, as well as temporarily blasting open a lowland dry-habitat, if badly scarred, corridor that allowed the species to move eastward. The populations in the Pacific region appear to have somehow managed to hang on in almost imperceptibly small numbers, because three individuals were documented by Dr. Campbell and colleagues in 1968–1969. These were overlooked museum specimens that had never been reported. Despite intense searches and extensive inquiries with locals, it appears that those populations finally succumbed to habitat loss and human persecution (these are venomous lizards, that people traditionally do not appreciate).

The genome tells us that there is a genetic signature of a current population of about 3,000 individuals. That number is most remarkable when considered in light of the actual number of lizards in the wild, based on field work mostly Dr. Ariano and colleagues, is only about 600 individuals. This significant mismatch is consistent with very recent (in geological time) declines in the population, and these losses are too recent to yet show signal in the genome. In other words, as human populations in present-day eastern Guatemala began to increase dramatically, this species suffered, again likely owing to habitat loss and human persecution. In a final bit of wisdom, Dr. Ariano made a most interesting connection. He realized that every indigenous human culture that occurred in the range of a species of beaded lizard portrayed the species in their artworks. For example, gila monsters are commonly portrayed in the historical and contemporary art and iconography of the Tohono O’odham culture. The same is true with other cultures throughout western Mexico, including Maya cultures in extreme southern Mexico. The Motagua Valley historically was a major cultural center for the Kiché Mayan people, whose

descendants still live there today. Yet, no trace of beaded lizards has ever been found among their ruins or recovered artworks. This is compelling, but admittedly indirect evidence, that when that culture was flourishing and building extensive cites and monuments about 2,500 years ago, the lizards simply were not there. This suggests that the lizards may have been in their current environment for a very short period of (geological) time. And, for the time being, they have nowhere else to go, as they are hemmed into their desert valley by unsuitable habitats of rainforest and cloudforest, and steep mountains around the valley.

This endangered lizard appears to have had a remarkable history, and conservationists in the U.S. and Guatemala are struggling valiantly to make sure that it survives our current human population levels. Please come visit our Guatemalan beaded lizards at Zoo Atlanta. They may look slow and sleepy—their general resting state—but they have a fascinating and complex story behind them. Thank you for your interest, and I will look forward to seeing you around the Zoo, perhaps on your next visit!

Joe Mendelson, PhD
Director of Research

Publication: Dyson, C. J., A. Pfennig, D. Ariano-Sánchez, J. Lachance, J. R. Mendelson III, and M. A. D. Goodisman. 2022. Genome of the endangered Guatemalan beaded lizard, Heloderma charlesbogerti, reveals evolutionary relationships of squamates and declines in effective populations sizes. G3 Genes|Genomes|Genetics 2022, jkac276. doi.org/10.1093/g3journal/jkac276

 

Left: The Guatemalan beaded lizard (Heloderma charlesbogerti) from Zoo Atlanta whose genome was assembled in our recent study (photos courtesy of M. Kern). Right: a topographic map of Guatemala (higher elevations are darker) with dots showing the current distribution of the species in the narrow, low-elevation Motagua Valley. The red triangle shows the location of of the Atitlan Volcano and the black arrow shows the probable route that its explosions opened up to allow the lizards to disperse into the Motagua Valley. Figure modified from Dyson et al., (2022).