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The Faculty of Arts and Sciences at Harvard University has a quaint but lovely tradition of reading a “memorial minute” to honor deceased members of the faculty. I recently came across the minute concerning Ernest Williams, which was presented in 2009 and published in the Harvard Gazette.

At a Meeting of the Faculty of Arts and Sciences on May 19, 2009, the following Minute was placed upon the records.

Ernest Williams was a man of many contrasts. Biology at Harvard in the third quarter of the last century was full of outsized personalities—titans in the field with strong opinions and no reservations about expressing them. In such company, Williams appeared a wallflower, seemingly wishing to be anywhere but in the midst of their arguments. Yet, one-on-one, Williams had an incisive wit and a dry sarcasm—discussions with him were always stimulating and provocative as he never missed a chance to challenge one’s thinking, sometimes quite pointedly.

To some, Williams’s work came across as old-fashioned. His subject, systematics — the study of the evolutionary relationships of species—is among the oldest in science, and his papers — florid and opinionated and, above all, long—recalled an approach to scholarship no longer in vogue. Yet much of his work was boldly innovative; some papers are still widely cited, and in several cases his work was well ahead of its time, presaging approaches to the study of evolutionary biology that were not to catch on for several decades.

Ernest Edward Williams was born January 7, 1914, in Easton, Pennsylvania, the only child of middle-aged parents. Like many boys, particularly of that time, he grew up loving nature and spent many hours capturing salamanders and other creatures. After attending Lafayette College, Williams joined the Army, serving in Europe during World War II. Upon his return, Williams entered graduate school at Columbia University, where he was the last graduate student of the great anatomist William King Gregory.

Williams’s doctoral thesis focused on the structure of the neck vertebrae of turtles and how variation among species reflects their evolutionary heritage. The work demonstrated the combination of careful attention to detail with the ability to interpret results in the broader context that was to characterize Williams’s career. More than fifty years later the work is still foundational in understanding the evolution of turtle diversity.

In 1950, after completing his degree, Williams moved to Harvard, where he initially served as a laboratory coordinator for the anatomy course of the legendary paleontologist Alfred Sherwood Romer, then subsequently was appointed as an assistant professor and made coordinator of a General Education course on evolution. The Museum of Comparative Zoology’s Curator of Herpetology, Arthur Loveridge, retired in 1957, and Williams was appointed to take his place.  In 1970 Williams rose to the rank of professor and in 1972 became Alexander Agassiz Professor of Zoology.

Williams initially focused on continuing his work on turtle systematics, leading to a series of publications including a still-important treatise published with Loveridge in 1957. Williams soon realized, however, that the museum’s collections were inadequate for the detailed analysis he conceived, which required large samples from many populations. This recognition that the museum’s herpetological collections were wide in scope, but lacking in depth, led Williams in two directions. First, it compelled him to work greatly to expand the Herpetology Department’s holdings, ultimately leading to a quadrupling of the department’s collections (to more than 300,000 specimens) by the time he retired as curator in 1980, making the Museum of Comparative Zoology (MCZ) one of the greatest herpetological repositories in the world. Second, it led Williams’s attention to focus on lizards in the genus Anolis, a very species-rich group from the Caribbean and Central and South America. A previous curator of herpetology and director of the MCZ, Thomas Barbour, had extensively collected anoles in the Caribbean; Williams, whose focus was much more evolutionarily-oriented than most systematists of the day, recognized that this group could be a model for studying large-scale evolutionary and biogeographical phenomena.

And, indeed, they were, and still are.

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Photo by Miguel Landestoy, from the New Yorker’s website

Well, actually it first came to light during a BBC expedition to film solenodons, but more recent legwork by AA  contributor Miguel Landestoy has rediscovered the animals near Pedernales in western Dominican Republic. Miguel’s efforts are chronicled in a delightful article in the New Yorker.

2014 was a good year for AA. 220,000 viewers in 195 countries (and that doesn’t count the 200 subscribers who get each post hand delivered to their email inbox–sign up now!*), 307 new posts, 1570 page views on one day. Guess which post that was? And who do you think the most frequent commenter was, with 76 comments? WordPress has kindly provided a list of information and stats, which you’re welcome to peruse.

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A new study out in Biology Letters by myself, Devi Stuart-Fox, Terry Ord and Indraneil Das found that two populations of the same species of gliding lizard – Draco cornutus – have diverged in gliding membrane colouration to match the colours of falling leaves in their respective habitats. An Anole Annals post by Ambika Kamath earlier this year looked at the study briefly after we’d spoken at the Animal Behaviour Conference in Princeton, but I thought I’d elaborate a little on working with Draco and how we devised the falling leaf camouflage hypothesis.

Figure 1. Draco cornutus at Bako National Park (photo credit– Devi Stuart-Fox)

Draco are small arboreal agamids, found throughout South-East Asia. They have extendable gliding membranes that they use for gliding between trees in their habitats. They also have dewlaps – like the Anoles – used in broadcast display to communicate with conspecifics. My work generally focuses on the diversity in dewlap colouration among species and how differences in habitat influence signal efficacy and may lead to speciation. This involves measuring the colours of lizards as well as taking behavioural footage of individuals of different species to look at how the patterns of display differ.

httpv://youtu.be/I_oeY9cIWOg

Footage by Terry Ord

Most Draco are very difficult to spot as they are well camouflaged and perch at least 3 metres high in their trees. Given this, searching for movement or displays are the best ways to locate an individual. Walking through the forest, we would often see in our periphery what we would initially dismiss as a falling leaf, only to later discover it was a gliding lizard. Indeed we quickly learnt to focus on ‘falling leaves’ when on the lookout for Draco and this was quite a fruitful approach. Indraneil Das was the first to suggest the gliding membranes were coloured to look like falling leaves – but it was a couple of years until we started to think about how we might test the idea. It became difficult to ignore how similar the fallen leaves on the ground at various study sites so closely resembled the colours and patterns of the gliding membranes of Draco species living in those immediate areas.

Then we made to trip to Niah Caves National Park in northern Borneo and came across a second population of D. cornutus.

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The big question–were they making s’mores?

The first anole paper of 2015 is a doozy. Everyone loves to roast marshmallows around a campfire. Turns out that “everyone” includes crested anoles, A. cristatellus! Read all about it in the paper by Norman Greenhawk in the new journal Life: the Excitement of Biology.

The uninformed often view parasites with disdain, disgust, and/or condemnation. These views however ignore the various ecological roles that parasites play. My colleagues and I are some of the lucky few who look at these organisms through ecological lenses and marvel at what we find.

An Anolis sagrei male from Chiayi County, southwestern Taiwan.

As part of the ongoing research on the exotic invasive brown anole (Anolis sagrei) populations in Taiwan, we collected and examined some specimens for parasites. In addition to the brown anoles, we also examined specimens of Eutropis longicaudata, Eutropis multifasciata, Japalura polygonata xanthostoma, Japalura swinhonis, Plestiodon elegans, and Sphenomorphus indicus, that were collected opportunistically from Taiwan.

We recently reported on the parasites we recorded in 52 of the 91 lizards examined, and the infected individuals harbored one to three species of parasites. We identified the parasites as Cyrtosomum penneri, Kiricephalus pattoni, Mesocoelium sociale, Meteterakis govindi, Oochoristica chinensis, Oswaldocruzia japalurae, Parapharyngodon maplestonei, Pseudabbreviata yambarensis, Pseudoacanthocephalus bufonis, or Strongyluris calotis. We also recorded an unidentifiable acanthocephalan infective juvenile (cystacanth) and an unidentifiable larva of a cestode (sparganum).

Based on the relatively few parasite species recorded from A. sagrei in Taiwan, compared to the large number of parasites reported from A. sagrei throughout its native and introduced range, it is clear that these lizards have been liberated from many of their parasites.

The nematode, Cyrtosomum penneri, which was introduced into Taiwan along with A. sagrei, was a common parasite in the A. sagrei we examined. None were recorded in any of the other lizard species examined. This is most likely because these nematodes are transmitted from one host to another during copulation and appears to have a fair degree of host specificity, so the spread of C. penneri to native lizard species in Taiwan is suggested to be very unlikely. An interesting conclusion that can be drawn from the presence of C. penneri in specimens from both the southwestern and eastern populations of A. sagrei in Taiwan is that sexually mature lizards were introduced into these localities and that they most likely have a common founder population.

Our study did also confirm that the digenean, Mesocoelium sociale, and the pentastome, Kiricephalus pattoni are acquired parasite of A. sagrei in Taiwan. Unfortunately, although their infections can be expected to be detrimental to the A. sagrei host, their infection frequencies are relatively low in the A. sagrei populations in Taiwan, and thus have no observed significant impact on the population sizes.

Another interesting finding of our study was that even though the nematodes, Pseudabbreviata yambarensis and Strongyluris calotis, are very common in Japalura swinhonis, a species that is very often sympatric with A. sagrei in Taiwan and which also has a very similar diet as A. sagrei, they have not been found in any of the A. sagrei examined to date. This could be a result of an absence of transmission routes that could be specific to J. swinhonis and thus protect introduced species from the native parasites, or the host-specific limitations of the parasites prevent them from adapting to a new hosts, i.e., A. sagrei.

I would like to encourage everyone involved with research to include parasitological studies in their herpetological works to expand our understanding of host-parasite ecology.

Photo by Julia Klaczko

This is an article wrtten by Stephanie Pappas and posted on livescience. It reports on a paper just published in the Journal of Zoology by Julia Klaczko, Travis Ingram, and me:

A lizard’s penis evolves six times faster than any of its other parts, a new study finds.

The study is the first to directly measure the evolution rate of the penis of any species, though researchers have long suspected that the male genitalia evolve faster than other body parts, said study researcher Julia Klaczko, a biologist at the University of Campinas in Brazil.

“What we see is, sometimes, very close species have very different hemipenes or genitalia,” Klaczko told Live Science. Hemipenes are the pair of organs that make up the version of a penis found in snakes and lizards. But dramatic genital differences are seen among closely related animals with penises, as well. [The 7 Weirdest Animal Penises]

Quick-changing penises

Because penises are often so different even in species that otherwise look almost identical, researchers frequently use genitals to discriminate between different species. Klaczko and her team chose to measure the genitals of 25 species of Anolis, a group of lizards that live in the Caribbean. Anolis lizards are a well-studied group, and researchers have lots of information about the relationships between the species, as well as their habitats and body shapes, Klaczko said.

The lizards’ hemipenes are tubular structures with a groove through which semen can flow. The researchers measured the length and width of the hemipenes in several specimens of each species. For comparison, they also measured the length of the lizards’ limbs, which evolve in response to the vegetation in the animals’ habitats, and the size of their dewlaps, which are the flaps of tissue near the throat that the lizards use for communication.

Next, using mathematical modeling, the researchers estimated the rates of evolution necessary to arrive at the differences in genitals, limbs and dewlaps. The result? Male genitalia change six times faster than either legs or throat flaps, making them more diverse in shape and size from one another than the other body parts.

Picky females or sexual warfare?

Klaczko and her colleagues aren’t sure what drives the rapid alterations in hemipenes. One possibility is that females pick mates with pleasing penises, whether that means their genitals are more stimulating or abetter “fit” in the female genitalia.

Another, less cooperative, possibility is that male and female lizards are locked in an evolutionary arm’s race in which both are trying to control reproduction. If this is the case, then males may be evolving genitals that give them an advantage in fertilization, while females evolve their genitals in an attempt to take that advantage back.

One known example of such a sexual arms race is the duck. Some duck species have corkscrew vaginas that spiral in the opposite direction of the males’ corkscrew penises, so the females can better resist unwanted mating attempts.

So far, the researchers haven’t studied female Anolis genitals, in part because vaginas are just harder to dissect and measure than hemipenes, Klaczko said. The next step, she said, is to try to understand the drivers in the variation in hemipenes’ shape and whether it has to do with differences in habitat, relationships between species, or some other factor.

The researchers reported their findings Jan. 5 in the Journal of Zoology.

Another news article on this research was just published on the Discovery News website.

Matt explains his methods.

The winner of this year’s Division of Ecology and Evolution Huey Award, Matt McElroy, gave an interesting presentation on gene flow and the Bogert Effect in Anolis cristatellus in Puerto Rico. Roughly, the Bogert effect says that thermoregulatory behaviors may shield a species from selection pressures on physiological processes experienced in different thermal environments. Therefore, divergent selection is expected to be weak in thermoregulating species, which can adjust their behavior to maintain a consistent body temperature in a range of thermal habitats. Alternatively, thermoconformers’ body temperatures match that of the environment, and so face strong divergent selection when exposed to new thermal habitats. Gene flow is expected to be high across thermal gradients for the thermoregulators and low for the thermoconformers.

Matt investigated the phylogeographic population structure and gene flow in A. cristatellus on the island of Puerto Rico, discovering three distinct populations. The southwestern population, in the arid rain shadow, was most divergent from the other two. He also conducted trasects up the mountain (a decreasing temperature gradient), finding that genes were moving out of the arid zones, but not the other way. If the Bogert effect held true, we would expect gene flow in both directions in this thermoregulating species; perhaps there is strong selection on cool adapted genotypes in warm habitats, but not vice versa. Matt suggested that higher population densities in lower elevations may influence the uni-directional flow, or that habitat destruction (e.g. hurricanes, agriculture) creates open, sunny patches, allowing the low-elevation populations (warm-adapted) to exploit elevations that they would not have been able to otherwise.

Photograph of a male Anolis sagrei from Christian Cox’s website.

Squamates vary widely in the magnitude and direction of body size dimorphism, which refers to the tendency for the sexes to exhibit different body sizes. Some lineages possess male-baised dimorphism while others have female-baised. The effects of testosterone on mediating sexual size dimorphism in different squamate lineages has long been the study of the Cox lab at the University of Virginia.  Christian Cox (of no relation to his advisor) has now reported some exciting steps forward in the search for the mechanisms regulating body size dimorphism in the brown anole, Anolis sagrei. Cox is in the process of carrying out a  transcriptome-wide analysis of the genes responsible for sexual dimorphism, with particular focus on examining the genes along the insulin growth factor-growth hormone axis (IGH-GH), which is the same pathway that was reported about yesterday.  In his experiment Cox implanted testosterone pellets under the skin of juvenile male and female lizards and then looked for differences in size and gene expression. Increased levels of circulating testosterone prompted increases in body size in both males and females grew to larger sizes, indicating that females have not lost the ability the respond to testosterone. But to better understand the growth axis controlling this difference Cox took a large step forward by also comparing gene expression in the liver of experimental (implant) and control (intact) animals. As the liver is a major regulator of growth via its regulation of the IGH-GH, Cox expected that this tissue would respond to testosterone treatment. This is precisely what Cox found. Specifically, he found a number of genes that are naturally regulated in different ways in males and females and additional genes that responded to the testosterone treatments. To conclude, Cox pointed out that an important next step will be to compare castrated lizards to those intact lizards with the testosterone implant to more clearly elucidate the gene network directly responding to testosterone. But perhaps the most exciting work will come with Cox and his collaborators examining the growth mechanisms of species with male-baised and female-baised patterns of dimorphism to more thoroughly understand how evolution has reshaped these gene regulatory networks during squamate evolution.

One of the largest anoles, Anolis equestris (photo by Uwe Bartlett)

From the diminutive twig anole to the monstrous crown-griant anoles, Anolis lizards vary dramatically in their body size. Much research has focused on the patterns of body size variation among Caribbean species, how changes in body size are correlated with habitat differences among species, and rates of body size evolution upon invasion to new islands, yet an important question remains to be addressed in this body of literature, “how do anoles change body size?” S. Griffis and Dr. D. Jennings of Southern Illinois University at Edwardville are attempting to address this among Cuban anoles by searching for DNA sequence differences in known growth factories. But they are using what might be considered an unlikely model for lizard body size variation: dogs. Several years ago, Elaine Ostrander’s lab at the NIH uncovered that coding differences in the growth factors IGF were responsible for the body size variation in dogs. To a mechanist like myself, it was a surprise that this variation could be traced to coding differences in the genes, not to the levels of circulating growth factors. The authors of this poster are following Ostrander’s lead by looking for coding differences in genes involved with the IGF growth axis. But to keep their options open they are also collecting data on circulating hormone levels. When complete, if there are differences in the IGF growth axis contributing to differences in body size, Griffis and Jennings will find it.