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In 1891, Elio Modigliani–an Italian biologist from Florence–collected an odd, male agamid lizard from northern Sumatra (type locality listed as “Si-Rambé Forest”). The specimen was brought back to Italy, and cataloged in the Museo Civico di Storia Naturale di Genova (Genova, Italy). More than 40 years later, this single specimen was described by Vinciguerra (1933) as Harpesaurus modiglianii. In his original description, Vinciguerra (1933) notes this Sumatran individual is a “notable lizard that is worth to be known,” and that it can be identified through a “[rostral appendage] as long as the head, simple, formed by a sickle-shaped compressed scale, upward and with its basis surrounded by some rather large scales” (Putra et al. 2020). It would be an injustice if I didn’t include the lovely plate featured in Vinciguerra’s original description (see below).

Vinciguerra’s 1933 illustration from his description of Harpesaurus modiglianii. After Modigliani’s collection of a single specimen, the species would be presumed extinct, and not seen again until 2018, just north of Toba Lake in Sumatra! The rediscovery was documented and published by Putra et al. (2020).

Though not seen again for another 129 years, Harpesaurus modiglianii is just one of several remarkable rostral appendage bearing lizards distributed throughout the world. Moreover, the story of H. modiglianii as an enigma to the herpetologists of Southeast Asia is not an unfamiliar one, as a congener–Harpesaurus tricinctus–faces a similar predicament, having not been seen since 1851! Still, importantly, interest in this group, and other rostral appendage bearing lizards, remains strong. As such, a critical question remains– just what exactly does the rostral appendage do? How might it relate to the ecology of these lizards? In a new paper in Salamandra, Ivan Ineich and colleagues discuss these topics exactly across a wide phylogenetic breadth, from Harpesaurus, to Calumma, to Anolis. Give it a read, and check out these amazing lizards!

 

New literature alert!

Pinocchio lizards and other lizards bearing rostral appendages − the peculiar habitus of the draconine agamid Harpesaurus tricinctus with highlights on its ecological implications and convergence with its New World equivalent, the dactyloid Anolis proboscis

In Salamandra

Ineich, Koppetsch, and Böhme (2022)

Abstract:

Vinciguerra, D. 1933. Descrizione di una nuova specie di Harpesaurus di Sumatra. Ann. Mus. civ. stor. nat. Genova 56: 355-357.

Harpesaurus tricinctus

I believe that several ways exist to do Science in Herpetology. Proposing and experimentally verifying hypotheses, for example, that a species is new to science, is one of them. But sometimes, important discoveries come out of nowhere, at least in appearance. In fact, they come from unrelated data and observations which, in certain circumstances, come together in a mind and lead to a concrete result.

I had the chance to make several discoveries of this nature during my career. The first concerns a very abundant and widely distributed small Pacific skink that everyone thought was a single species, Emoia cyanura. By observing several thousand specimens in the laboratory, I noted certain morphological and coloring characters whose presence varied from one individual to another, but many were linked to each other. I left it at that, but once in the field in French Polynesia a few years later, very quickly I realized that all these characters made it possible to highlight two sympatric, but not quite syntopic, species that everyone was confusing until my thesis work in 1987. Immense pleasure!

The second discovery is that of an external supralabial gland whose excretion orifice is visible in all snakes of the genus Echis. Hundreds of herpetologists have counted the supralabial scales in these snakes without seeing this orifice, which is so obvious now.

The third discovery in my career as a herpetologist is that of Bocourt’s terrifying skink (Phoboscincus bocourti). It was on a small tiny island in New Caledonia that I found, in 2003, a very large lizard that had been considered extinct for almost 150 years. Never such a discovery was imaginable, even less in this small place yet already explored by herpetologists.

Harpesaurus tricinctus MNHN 0623 HOLOTYPE

Now let’s see my fourth and most recent discovery. Being responsible for the collections of squamate reptiles at the National Museum of Natural History in Paris from 1988 until 2014, I often took photographs of lizards to respond to requests from colleagues. This is how, at the beginning of my career, I was asked to photograph a very original little Asian draconine agamid due to the presence of a relatively long flexible rostrum at the front of its head. The origin of this unique specimen is obscure because only “Java” is indicated without a collector’s name. Auguste Duméril described this specimen in 1851 as a new species, Harpesaurus tricinctus. There is a vellum which represents this lizard still relatively fresh with some colors preserved. The lizard has never been found since and is considered extinct.

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In December 2016 I was looking at issue 4 of volume 47 of Herpetological Review. In this issue, an advertisement for the 11th Latin American Congress of Herpetology in Quito, Ecuador was illustrated with a photograph of a strange lizard that immediately caught my eye. I really thought I was dreaming when I saw this image. This lizard looked almost totally like H. tricinctus, yet it was a South American species! At first, I thought that Duméril was mistaken and that his Asian agamid was a South American dactyloid. Examination of complementary material in the collections quickly showed that these were indeed two distinct species from different families, one Asian (Agamidae) and the other South American, Anolis proboscis (Dactyloidae). The latter was long, mysterious and no data were published on its ecology until 2007. From that year, the species was rediscovered and its ecology described. I then thought that this extreme convergence reflected a quite comparable ecology between A. proboscis and H. tricinctus, the latter being considered extinct. The written article was submitted to the Raffles Bulletin of Zoology in 2019 but was not accepted even before its passage by the reviewers. I then contacted Wolfgang Böhme and Thore Koppetsch, who were enthusiastic to join me in completing this project. Both have completed my work and this association has allowed its publication in the famous journal Salamandra in May 2022 (available here). The well-known ecology of the first lizard should make it possible to rediscover the Asian agamid and make it a Lazarus species. Another species of the genus, Harpesaurus modiglianii, was rediscovered in Sumatra in 2020, after almost 130 years without observation. All hopes are therefore allowed to find H. tricinctus based on the ecological information obtained from its convergent dactyloid.

Anolis proboscis. Photo by Jonathan Losos

All the data resulting from this work is available in:

Ineich I, Koppetsch T, Böhme W. 2022 – Pinocchio lizards and other lizards bearing rostral appendages − the peculiar habitus of the draconine agamid Harpesaurus tricinctus with highlights on its ecological implications and convergence with its New World equivalent, the dactyloid Anolis proboscis. Salamandra 58(2):123-138.
https://www.researchgate.net/profile/Ivan-Ineich/research

Picture of a female A. sagrei with the diamond pattern.

Readers of this blog will be well aware of the conspicuous variation in dorsal color patterns of Anolis lizards – think of the spots of A. sabanus, or the bands of A. transversalis (both worthy a google search if you happen to be unfamiliar with them). Such patterns are particularly interesting when several patterns exist within a single population – a polymorphism. This is the case in A. sagrei where females have either a chevron-like pattern, same as all males of this species, or a diamond-like pattern on their backs.

In 2016, I visited some A. sagrei populations in Florida and became interested in this female-limited color pattern polymorphism. Being a developmental biologist, what puzzled me most was not if selection can maintain multiple patterns, but how the two patterns actually develop.

On the one hand, the difference between the two patterns ought to have a simple genetic basis. Diamond- and chevron-females mix within the same population and the two morphs are discrete (although there is a continuous variation within both morphs, and the diamonds sometimes look more like a band [1]). On the other hand, the developmental biology of pattern formation is far from trivial. Here is a little teaser of the complexity: in vertebrates, pigment cells are derived from neural crest cells that originate along the dorsal midline of the early embryo. Once detached from the crest of the neural tube, pigment cell precursors migrate towards their final destination in the epidermis, where they differentiate into pigment cells – xanthophores, melanophores and iridophores. What these cells do and how they organize themselves are what gives rise to patterns. And this does not seem to be very simple at all. So how can we reconcile a simple genetic basis with the complex developmental biology of pattern formation of diamonds and chevrons?

The two female morphs and a male of A. sagrei.

Simply out of curiosity, we set out to solve this puzzle. Thanks to our anole breeding group at Lund University, we already had three generations of A. sagrei of both morphs that we could use to address the pattern of inheritance of diamonds and chevrons, and to identify the underlying gene(s). Our intuition about the simple genetic architecture of the polymorphism held true, and we identified a single Mendelian locus that perfectly segregated with the morph patterns.

Surprisingly though, the locus was not on a sex chromosome, so this could not explain why only females are polymorphic. Instead, the identity of one of the two genes located at the Mendelian locus pointed to a solution: the estrogen receptor 1 gene is crucial for the development of female traits and therefore expressed at higher levels in females compared to males. Because of the close physical proximity of the two genes at the Mendelian locus, also the second gene shows a female-biased expression pattern. So while the estrogen receptor 1 gene does not explain the pattern differences, it explains why the polymorphism is only present in females.

But what is this second gene at the Mendelian locus, and how does it explain the difference in patterning? It is a gene encoding the coiled-coil domain-containing protein 170, or CCDC170. Not exactly a usual suspect of color pattern formation. In fact, not much is known about this gene, but the cancer literature had demonstrated that it codes for a structural protein that regulates the migratory capacity of cells (mutations in CCDC170 can make cancer cells migratory and are associated with an aggressive type of breast cancer). The proteins encoded by the diamond and chevron alleles were predicted to form CCDC170 proteins with structural differences. This is likely to affect the function of the protein – perhaps by influencing migratory behaviors of pigment cell precursors.

Testing this hypothesis is easier said than done. As a first proof-of-principle, we used an in silico modelling approach to test if tinkering with the migratory capacity of cells can switch a system from generating chevron-like to diamond-like patterns. Miguel Brun-Usan is a magician with cell-based computer modelling and his trick is to create computer models that are complex enough to capture real biological phenomena, yet simple enough to allow us to trace and understand what is going on. To get to the bottom of the diamond/chevron morph differences, he implemented cells on a growing epithelium with a Turing-type mechanism consisting of a gene regulatory network (GRN) with up to five genes. By running a number of experiments (yes, computer scientists also run experiments, I learned), Miguel could demonstrate that some GRNs generated back patterns that very much resembled those of real lizards. Moreover, he found that modifying a single gene in the GRN that regulates the migratory capacity of cells is sufficient to switch the system from generating chevrons (if migration is switched ON) to diamonds (if migration is switched OFF).

A brief graphical abstract of our study.

So it seems that what reconciles the simple genetic basis of the polymorphism with the complex process of pattern formation is that the underlying developmental system exhibits a high degree of controllability. Simply modifying migratory capacities of cells by tinkering with one gene in the core GRN leads to changes in collective cell migration, visible as a distinct and new dorsal color pattern. Such high controllability could explain the evolvability of dorsal color patterns and result in high turn-over rates between patterns, as beautifully demonstrated by geckos [2]. I am excited to continue this research to see if the model can be substantiated mechanistically. I would also like to test if convergent evolution of diamond patterning in different Anolis species is underpinned by convergent developmental and genetic mechanisms. If you are interested in joining our research group, please get in touch (nathalie.feiner@biol.lu.se; www.feiner-uller-group.se).

You can read the full article here:

Feiner, N., M. Brun-Usan, P. Andrade, R. Pranter, S. Park, D. B. Menke, A. J. Geneva, and T. Uller. 2022. A single locus regulates a female-limited color pattern polymorphism in a reptile.
Science Advances 8:10 DOI: 10.1126/sciadv.abm2387

Other references:

• Moon, R.M., and Kamath, A. (2019). Re-examining escape behaviour and habitat use as correlates of dorsal pattern variation in female brown anole lizards, Anolis sagrei (Squamata: Dactyloidae). Biol J Linn Soc 126, 783-795.
• Allen, W.L., Moreno, N., Gamble, T., and Chiari, Y. (2020). Ecological, behavioral, and phylogenetic influences on the evolution of dorsal color pattern in geckos. Evolution 74, 1033-1047.

Anolis porcatus is the most recent Caribbean anole to have been documented to consume and disperse seeds. Natural history research by Armas (2022) observes A. porcatus feeding on West Indian holly, and finds successful germination of the fecal pellets. Credit Thomas Brown (Wikimedia Commons).

Recent research on Anolis lizards has suggested their omnivorous tendencies might aid in the dispersal of seeds. Most recently, this was discussed by Giery et al. (2017), who reported Cuban Knight Anoles (A. equestris) to consume and disperse royal palms. This year, Armas (2022) reports Anolis porcatus consumes and disperses West Indian holly. Check it out!

New literature alert!

Consumption and Dispersal of West Indian Holly (Turnera ulmifolia, Turneraceae) Seeds by Cuban Green Anoles, Anolis porcatus (Squamata: Dactyloidae)

In Reptiles & Amphibians

Armas (2022)

Literature Cited:

de Armas, L. F. (2022). Consumption and Dispersal of West Indian Holly (Turnera ulmifolia, Turneraceae) Seeds by Cuban Green Anoles, Anolis porcatus (Squamata: Dactyloidae). Reptiles & Amphibians, 29(1), 115-116.

Giery, S. T., Vezzani, E., Zona, S., & Stroud, J. T. (2017). Frugivory and seed dispersal by the invasive knight anole (Anolis equestris) in Florida, USA. Food Webs, 11, 13-16.

Photo from http://www.petworldshop.com/

Nigel Rothfels, a historian of animals and culture at the University of Wisconsin-Milwaukee, asks:

Given the previous AA post on anoles in the pet trade, the amount of in-country breeding there must be of anoles, the general life-span of anoles, and the general growth in pet-keeping since Covid, what is your highly educated guess on the number of anoles currently being kept in captivity world-wide (as pets, for educational supply companies, in labs, or zoos).  With 350,000/year being collected in just Louisiana in 2006, it makes me think that something like 3-5 million might still be an underestimate.

Anyone want to venture an estimate?

This year at SICB, I had the great opportunity to talk about part of my work as a postdoctoral researcher in the lab of Dr. Michael Logan at the University of Nevada, Reno. In collaboration with John David Curlis (University of Michigan), Christian Cox (Florida International University), W. Owen McMillan (Smithsonian Tropical Research Institute), and Carlos Arias (STRI), we have been studying the Panamanian slender anole Anolis apletophallus, which has a dewlap polymorphism: males either have a solid orange dewlap (solid morph) or a white dewlap with an orange spot (bicolor morph). Preliminary results from John David Curlis’ PhD dissertation research suggests that, in our mainland study population, the frequencies of these morphs change in conjunction with understory light levels—the solid morph is more frequently observed in brighter areas where more light reaches the understory, whereas  the opposite is true for the bicolor dewlap, which is more frequently observed in darker areas of the forest. Thus, it seems possible that selection is maintaining this polymorphism following the predictions of the sensory drive hypothesis, which states that sexual signals should have characteristics that make them the most transmissible given the physical characteristics of the local habitat.

As part of an effort to understand how this trait is evolving in the wild, I set out to understand the genetic basis of this dewlap polymorphism. To do this, my collaborators and I first assembled the full slender anole genome which we then used as a reference for a pooled population sequencing (Pool-Seq) approach using half individuals with solid dewlaps and half individuals with bicolor dewlaps to identify the genomic region underlying this dewlap polymorphism.

Our genome assembly showed pretty good results (Scaffold N50 154,613,287). The Pool-Seq results presented a clear peak of differentiation between solid and bicolor morph groups that corresponded to a region on Scaffold 3. We have a promising candidate gene within this region that may underly the dewlap polymorphism, but will continue to explore these data further to understand the genetic basis of this charismatic trait.