Category: New Research Page 8 of 66

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The adhesive structures of geckos have been the subject of extensive inquiry across a variety of disciplines ever since Autumn et al. (2002) discovered that van der Waals intermolecular forces are the main driver of gecko adhesion. Geckos adhere to surfaces using expanded subdigital scales (scansors/lamellae) that are covered in thousands of beta-keratin fibrils (setae) that branch into hundreds or thousands of triangular-shaped tips (spatulae) that are about 200 nanometers in width (see slideshow for images). Spatulae make intimate contact with a surface resulting in van der Waals intermolecular forces. Gecko adhesive toe pads are multifunctional; they are a reversible dry adhesive, they can adhere to a variety of surfaces, they can adhere underwater in some conditions, they have self-cleaning and self-drying capabilities, and they can adhere in a vacuum (see Autumn et al. 2014 for a recent review of gecko adhesion). A number of gecko-inspired synthetic adhesives have been generated over the years, but have not yet managed to replicate the multifunctionality observed in the natural system (Niewiarowski et al. 2016). There are a number of potential explanations for this, but one could be that most gecko-inspired synthetic adhesives are simplified single fibers that do not fully replicate the multiply branched structure of gecko setae. Anoles, however, have independently evolved adhesive toe pads with fundamentally simpler microstructures compared to their gecko counterparts; anole setae are single fibers with a single, larger spatulate tip and more closely resemble the gecko-inspired synthetic adhesives that are currently capable of being generated (see slideshow for images). Therefore, anoles may be an excellent model fibrillar system to better understand the observed functional discrepancy between synthetic and natural fibrillar adhesives.

In an invited paper recently accepted for publication in Integrative and Comparative Biology, my co-authors and I (see full citation below) briefly reviewed the relevant literature concerning the anole adhesive system, discussed how investigation of this convergently evolved system could impact our general understanding of fibrillar adhesion, and suggested a number of hypotheses and areas of future inquiry that could be tackled in future work.

Anole adhesive toe pads have often been suggested as evolutionary key innovations (Losos 2011), yet they have not been nearly as well studied as gecko adhesive toe pads. Nevertheless, general morphometrics, clinging ability on smooth substrates, and correlations between adhesive toe pad size, clinging ability, and habitat use have been reported for anoles (Losos 2011). Studies, however, reporting Anolis clinging ability on ecologically-relevant surfaces, detailed morphometric data of anoline setae, and the multifunctional properties of anoline adhesive toe pads are limited or nonexistent. Anoles may be excellent models for fibrillar adhesion for four main reasons: (1) anole setae are closer in dimensions and morphology to the currently producible gecko-inspired synthetic adhesives, (2) anole setae are not multiply branched which may reduce the complexity of modeling and/or explaining adhesion especially under non-ideal circumstances, (3) anole setae also more closely resemble the theoretical models previously used to explain gecko adhesion, and (4) the extensive evolutionary and ecological data on anoles may assist in answering persisting questions regarding the adhesion ecology and evolution of adhesive pad-bearing lizards.

Although the gecko adhesive system has been particularly well-studied over the past two decades, many fundamentals of biological fibrillar adhesion still need to be worked out or are otherwise unknown. We believe that parallel investigation of the anoline fibrillar adhesive system may assist in filling these gaps in our knowledge, and thus we encourage an interdisciplinary, communal effort to investigate the adhesive ecology, evolution, morphology, performance, and behavior of anoles.

Full citation

Garner, A.M., M.C. Wilson, A.P. Russell, A. Dhinojwala, and P.H. Niewiarowski. Going Out on a Limb: How Investigation of the Anoline Adhesive System can Enhance our Understanding of Fibrillar Adhesion. Integrative and Comparative Biology. In press. Link to article.

References

Autumn K, Niewiarowski PH, Puthoff JB. 2014. Gecko Adhesion as a Model System for Integrative Biology, Interdisciplinary Science, and Bioinspired Engineering. Annual Review of Ecology, Evolution and Systematics 45(1):445-470.

Autumn K, Sitti M, Liang YA, Peattie AM, Hansen WR, Sponberg S, Kenny TW, Fearing R, Israelachvili JN, Full RJ. 2002. Evidence for van der Waals adhesion in gecko setae. Proceedings of the National Academy of Sciences, USA 99(19):12252-12256.

Losos JB. 2011. Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California Press.

Niewiarowski PH, Stark AY, Dhinojwala A. 2016. Sticking to the story: outstanding challenges in gecko-inspired adhesives. Journal of Experimental Biology 219(7):912-919.

Leptin is made by fat cells and serves as a signal of available energy to lots of systems in the body. Diagram from healthjade.com

When you only have so much money to spend, you have to carefully consider what you’ll use it for. Do you go for instant gratification (dinner at your favorite, but expensive, restaurant!), or do you invest in something with a longer-term return (a needed kitchen appliance that will last years)? Free-living organisms have to make this choice throughout their lives. Of course they don’t cook in a kitchen, but their bodies have to ‘decide’ what to do with precious and limited energy. For our beloved anoles, in what do they invest that hard-earned energy from ingested bugs? Make more and bigger babies right away? Grow more? Invest in their immune system or locomotor performance to survive better?

Animal bodies don’t actually make ‘decisions’ about these things. Instead, hormonal and molecular mechanisms are arranged as networks in the body to make ‘decisions’ under different sets of conditions. In a new paper, Andrew Wang, a recent graduate from Jerry Husak’s lab, was curious how such decisions are made in green anoles. Previous work in the Husak lab showed that when calories are restricted, and lizards are forced to invest in athleticism via exercise training, both reproduction and immune function suffer. Why is that, and is it reversible?

The observation that trained and food-deprived lizards had little to no body fat (imagine elite marathon runners!) suggested that the hormone leptin, produced by fat cells, might be responsible. Leptin affects lots of systems in the body (see figure above), and less fat means less leptin. This means that leptin serves as a direct and convenient signal of energy stores: if you have enough energy, then you can direct organs to get to work. This fact has led to a huge literature on how leptin, as an energy signal, controls tradeoffs among traits. Hopefully you’re seeing a slight paradox here – if more leptin means more energy available, how could it mediate tradeoffs? How do you get more of one trait than another if leptin controls both in the same general direction?

Andrew conducted an experiment to find out. He replicated previous work, training and calorie restricting male and female green anoles to cause suppressed reproduction and immune function. He then gave half supplemental leptin and the other half saline, expecting leptin to ‘rescue’ reproduction, immunity, or both. The results were clear: immunity was ‘rescued,’ but reproduction was not. That is, both sexes were investing in survival-related traits to (hopefully) reproduce later instead of just reproducing right away. These results suggest that either there wasn’t enough energy for reproduction and the signal was moot, or the two traits have different sensitivities to leptin. Future work will help to disentangle these possibilities, but this work gives us more understanding of how anoles allocate energy when it’s limited.

Figure from Wang et al. (2019). Key: U=untrained, T=trained, H=high diet, R=restricted diet, L=leptin injected, S=saline injected. Note here that the swelling response to PHA injection was suppressed with training and caloriee restriction, but it was rescued with leptin (T-R-S vs T-R-L).

Paper: Wang AZ, Husak JF, Lovern M. 2019. Leptin ameliorates the immunity, but not reproduction, trade-off with endurance in lizards. J Comp Physiol B, in press. doi: 10.1007/s00360-019-01202-2

Figure 1 . (A) Widespread species may be comprised of populations (dashed lines) exhibiting traits generalized across all habitats or (B) capable of specializing to unique habitats throughout their range.

Widespread species are expected to be successful in natural environments because of their ability to generalize across a variety of habitats. Throughout their range, widespread species may experience a variety of habitat types and may subsequently exhibit similar patterns of morphology and performance capabilities. In this sense, widespread species could encounter a “jack-of-all trades but master of none” trade-off in that a population may not be optimally adapted to a certain environment (Figure 1A). By contrast, we hypothesized in a recent paper published in Evolution that local specialization could be driving the broad-scale success of a widespread species. By adapting to a specific habitat, natural selection could produce unique fitness surfaces and phenotypic variation between populations (Figure 1B).

In this study, my collaborators and I conducted this study on four distinct populations of Urosaurus ornatus, a widespread lizard found throughout the American southwest (Figure 2), to determine whether success is a result of ecological generalism or local specialization. Urosaurus ornatus is a small, polymorphic lizard that primarily occupies desert habitats. While the common name is the ornate tree lizard, this species can naturally be found on a wide variety of substrates, including tree limbs, tree trunks, boulders, shrubs, snags, canyon walls, and the ground. We focused on populations found in one of two microhabitat types, tree-dominated or boulder-dominated, to assess habitat-specific differences in natural selection.

Figure 2. Male (left) and female (right) Urosaurus ornatus on a natural perch.

Morphological characters and performance capacity are ideal traits for this experiment due to their sensitivity to ecological and environmental characteristics. Thus, our results show striking differences in selection on these traits by sex, supporting the notion of divergent ecological pressures within a shared environment. This, coupled with the heterogeneity in selection between habitat types, leads us to believe that local adaptation is driving the success of this widespread species. In the past, evidence for generalism at the species level has masked the underlying affects of the environment and local adaptation. Here we are able to tease apart some of these traits and determine how selection varies at the population level in order to extrapolate to the species level.

So what do tree lizards have to do with anoles? In short, the similarities between Urosaurus and Anolis are plentiful. While there may be significant differences in habitat, both genera contain species that are wonderful models for a plethora of different ecological, evolutionary, and genomic questions. The wide breadth of anole literature has influenced our findings in this study and contributed significantly to its impact and viability. For that, we thank the many anole researchers from around the world!

The somatropic axis regulates growth in vertebrates

Our growth during development is controlled by a complex brain-body axis called the somatotropic axis. Put simply as in the photo below, the hypothalamus in the brain signals the pituitary to release growth hormone into the body where it stimulates the liver to produce two forms of insulin-like growth facts (IGF1 and IGF2). Both growth hormone and IGF have different effects on growth of muscle and bone. While we rely on mouse models to study how IGF might impact human development, it turns out that the relative secretion of IGF1 and IGF2 over the course of life is quite different in the two species. In fact, we know little about IGF production and signaling in non-mammals.

Expanded view of the somatotropic axis to show receptors and binding proteins. From Yakar et al. (2018).

Abby Beatty, from Tonia Schwartz’s lab at Auburn University, set out to determine the developmental pattern of the somatotropic axis in brown anoles. Of course, the axis is much more complex than the diagram above, including receptors in various tissues, binding proteins that carry the signals around the body (see below), and proteins in cells that cause responses (IRSs). Abby studied expression of IGF1, IGF2, and five binding proteins during brown anole development, from embryo to hatchling to adult. She expected to find that IGF1 and 2 would be expressed differentially and that the expression patterns would differ across life stages. That’s exactly what she found. IGF1 and 2 were both low and similar in expression early in development, but at hatching IGF increased with IGF2 expressed more than IGF in adults. Surprisingly this is more like a human pattern than a mouse is!

As for the binding proteins, expression was similar for all of them in the brain, gonads, and liver, but BP3 was expressed less in the heart. It’s still unclear what these patterns in binding proteins mean for brown anole development, but they make for some excellent future research questions! Indeed, these results add to the already-long list of things that makes anoles good model systems.

Christine Rohlf from the University of St. Thomas presents her research on immune-performance tradeoffs.

Traveling to SICB is always exciting, but like any trip through crowded airports, hotels, and convention centers, you’re more likely to get sick during your travel if you’re not careful. As we all know, getting a travel cold (or worse) makes you feel terrible and certainly doesn’t make you want to run on a treadmill! The same is likely true in wild animals, including anoles. Mounting immune responses is energetically expensive, but so are other things that lizards have to do, like forage, escape predators, and process food. So, does an increasingly large immune challenge decrease a lizard’s ability to perform? Christine Rohlf, an undergraduate student in Jerry Husak’s lab at the University of St. Thomas, wanted to find out in green anoles.

Christine designed a laboratory experiment to determine whether two types of immune challenge, alone and in combination, decreased bite-force performance, sprint speed, or endurance capacity compared to controls. Some lizards received two sequential injections of lipopolysaccharide (LPS), some received a skin wound with a biopsy punch, and some received both. LPS is a signal on gram-negative bacteria that, when injected, tricks the body into thinking it is infected with bacteria. So, you get an immune response, but you don’t actually get an infection.

Surprisingly, none of the immune challenges affected sprint speed or endurance compared to controls. Although the lizards were not calorie-restricted, they were on a modest diet, meaning that energy was limited, but clearly not enough to make a difference. Apparently these two immune challenges aren’t as costly as we thought. The only effect that Christine found was that the second LPS injection significantly decreased bite force. Because bite force is likely the least energetically expensive trait of those measured (imagine running until you’re exhausted versus biting into a hard piece of French bread), Christine suspects that the decrease in bite force was due to a lack of motivation while feeling sick. Future work with calorie-restricted lizards should tell us if mounting an immune challenge is a significant cost to anoles.

Amy Payne of Trinity University presents her research on tail autotomy in 7 lizard species.

One of the most interesting features of many lizards, including anoles, is that they can willingly, and actively, lose their tails to escape predators. While it might seem counterintuitive to lose a large body part, it’s better than being eaten! Despite the obvious benefit of surviving another day, there are some costs associated with tail autotomy.

Amy Payne, a student in Michele Johnson’s lab at Trinity University of San Antonio, wanted to know whether the frequency of tail loss across seven species was associated with predatory and social use of the tail as well as energetic content of the tail. For those that are anole-inclined (which is why you’re here), Amy included A. cristatellus and A. carolinensis. She caught and measured hundreds of lizards, and made behavioral observations on them as well. She was then able to quantify how many lizards of each species had a lost/regenerated tail, as well as what proportion of each tail was lost.

Surprisingly, frequency of tail loss was not associated with using the tail in a social or predatory context. However, there was an association between these two functions of the tail: species that more often used their tail for predatory use also used their tail in social contexts more. There was no relationship between the frequency of tail loss and the proportion of the tail that was lost on average across species. But she did find some really cool results when looking at energetic content of the tail. Amy found that there was a significant positive relationship between frequency of tail loss and tail energy content. That is, the more energy that lizards have in their tails, the more frequently individuals in that species will have a lost/regenerated tail. While this seems opposite to what one might casually predict, Amy hypothesizes that the predator-distraction to survive function of tail autotomy is more likely to succeed if the tail is larger and more beneficial to the predator. In other words, if a lizard has a scrawny tail and drops it off for a predator, it is more advantageous for the predator to ignore the low-cal tail and just eat the lizard. This would put selection on species with low-energy content tails to be more prudent about when they drop their tails. These really interesting results open up some exciting areas for future research on the costs and benefits of tail autotomy!