Macroevolutionary diversification of glands for chemical communication in squamate reptiles

Chemical communication plays a central role in social, sexual and ecological interactions among animals. However, the macroevolutionary diversification of traits responsible for chemical signaling remains fundamentally unknown. Most research investigating evolutionary diversification of glands responsible for the production of chemical signals has focused on arthropods, while its study among vertebrates remains neglected. Using a global-scale dataset covering > 80% (7,904 species) of the living diversity of lizards and snakes (squamates), we investigate rates, trajectories and phylogenetic patterns of diversification of their follicular glands for chemical communication. We observed these glands in 13.66% of species, that their expression has varying phylogenetic signal among lineages, and that the crown squamate ancestor lacked follicular glands, which therefore originated and diversified subsequently during their evolutionary history. Additionally, our findings challenge the longstanding view that within squamates the Iguania are visually oriented while Scleroglossa are chemically-oriented, given that Iguania doubles Scleroglossa in the frequency of glands. Our phylogenetic analyses identified stabilizing selection as the best model describing follicular gland diversification, and revealed high rates of disparity. We provide the first global-scale analysis investigating the diversification of one of the main forms of communication among reptiles, presenting a macroevolutionary angle to questions traditionally explored at microevolutionary scale

The macroecology of chemical communication in lizards: do climatic factors drive the evolution of signalling glands?

Chemical communication plays a pivotal role in shaping sexual and ecological interactions among animals. In lizards, fundamental mechanisms of sexual selection such as female mate choice have rarely been shown to be influenced by quantitative phenotypic traits (e.g., ornaments), while chemical signals have been found to potentially influence multiple forms of sexual and social interactions, including mate choice and territoriality. Chemical signals in lizards are secreted by glands primarily located on the edge of the cloacae (precloacal glands, PG) and thighs (femoral glands), and whose interspecific and interclade number ranges from 0 to >100. However, elucidating the factors underlying the evolution of such remarkable variation remains an elusive endeavour. Competing hypotheses suggest a dominant role for phylogenetic conservatism (i.e., species within clades share similar numbers of glands) or for natural selection (i.e., their adaptive diversification results in deviating numbers of glands from ancestors). Using the prolific Liolaemus lizard radiation from South America (where precloacal glands vary from 0-14), we present one of the largest-scale tests of both hypotheses to date. Based on climatic and phylogenetic modelling, we show a clear role for both phylogenetic inertia and adaptation underlying gland variation: (i) solar radiation, net primary productivity, topographic heterogeneity and precipitation range have a significant effect on number of PG variation, (ii) humid and cold environments tend to concentrate species with a higher number of glands, (iii) there is a strong phylogenetic signal that tends to conserve the number of PG within clades. Collectively, our study confirms that the inertia of niche conservatism can be broken down by the need of species facing different selection regimes to adjust their glands to suit the demands of their specific environments

Supplementary material from "Upper beak depression instead of elevation dominates cranial kinesis in woodpeckers"

The value of birds’ ability to move the upper beak relative to the braincase has been shown in vital tasks like feeding and singing. In woodpeckers, such cranial kinesis has been thought to hinder pecking as delivering forceful blows calls for a head functioning as a rigid unit. Here, we tested whether cranial kinesis is constrained in woodpeckers by comparing upper beak rotation during their daily activities such as food handling, calling and gaping with those from closely related species that also have a largely insectivorous diet but do not peck at wood. Both woodpeckers and non-woodpecker insectivores displayed upper beak rotations of up to 8 degrees. However, the direction of upper beak rotation differed significantly between the two groups, with woodpeckers displaying primarily depressions and non-woodpeckers displaying elevations. The divergent upper beak rotation of woodpeckers may be caused either by anatomical modifications to the craniofacial hinge that reduce elevation, by the caudal orientation of the mandible depressor muscle forcing beak depressions, or by both. Our results suggest that pecking does not result in plain rigidification at the upper beak's basis of woodpeckers, but it nevertheless significantly influences the way cranial kinesis is manifested.Este conjunto de datos es el material suplementario del artículo citado, al que puede accederse en "Documentos relacionados".Fil: Lyons, Sebastián. Universidad Nacional de La Plata. Facultad de Ciencias Naturales y Museo; Argentina.Facultad de Ciencias Naturales y Muse

Chemical signalling in lizards: an interspecific comparison of femoral pore numbers in Lacertidae

Animals communicate via a variety of sensory channels and signals. Studies on acoustic and visual communication systems suggest that differences in the physical environment contribute to the variety of signalling behaviour, with species investing in those signals that are transmitted best under the local conditions. Whether or not environmental tuning also occurs in chemical communication systems has received much less attention. In the present study, we examined the effect of several aspects of the physical environment on the chemical communication system of lacertid lizards (family Lacertidae). The numbers of femoral pores are used as a proxy reflecting how much a particular species invests in and relies upon chemical signalling. Femoral pores are specialized epidermal structures that function as a secretion channel for the waxy substance produced by glands. In some lacertid species, the secretion carries infochemicals that play an important role in social communication. The number of femoral pores varies considerably among species. We have compiled data on femoral pore numbers for 162 species and tested for the effects of climate and substrate use. After correcting for body size and taking the phylogenetic relationships among the species into account, we found no effect of climate conditions or latitude on species pore numbers. Substrate use did affect pore numbers: shrub-climbing species tended to have fewer femoral pores than species inhabiting other substrates

How to behave when marooned: The behavioural component of the island syndrome remains underexplored

Animals on islands typically depart from their mainland relatives in assorted aspects of their biology. Because they seem to occur in concert, and to some extent evolve convergently in disparate taxa, these changes are referred to as the island syndrome'. While morphological, physiological and life-history components of the island syndrome have received considerable attention, much less is known about how insularity affects behaviour. In this paper, we argue why changes in personality traits and cognitive abilities can be expected to form part of the island syndrome. We provide an overview of studies that have compared personality traits and cognitive abilities between island and mainland populations, or among islands. Overall, the pickings are remarkably slim. There is evidence that animals on islands tend to be bolder than on the mainland, but effects on other personality traits go either way. The evidence for effects of insularity on cognitive abilities or style is highly circumstantial and very mixed. Finally, we consider the ecological drivers that may induce such changes, and the mechanisms through which they might occur. We conclude that our knowledge of the behavioural and cognitive responses to island environments remains limited, and we encourage behavioural biologists to make more use of these natural laboratories for evolution'. © 2022 Royal Society Publishing. All rights reserved

Protein–lipid Association in Lizard Chemical Signals

[EN] Chemical communication in terrestrial vertebrates is often built on complex blends, where semiochemical and structural compounds may form an integrated functional unit. In lizards, many species have specialized epidermal glands whose secretions are waxy, homogeneous blends of lipids and proteins, both active in communication. The intimate co-occurrence of such compounds allows us to hypothesize that they should undergo a certain degree of covariation, considering both their semiochemical role and the support-to-lipid function hypothesized for the protein fraction. In order to assess the occurrence and level of protein–lipid covariation, we compared the composition and complexity of the two fractions in the femoral gland secretions of 36 lizard species, combining phylogenetically-informed analysis with tandem mass spectrometry. We found the composition and complexity of the two fractions to be strongly correlated. The composition of the protein fraction was mostly influenced by the relative proportion of cholestanol, provitamin D 3 , stigmasterol, and tocopherol, while the complexity of the protein pattern increased with that of lipids. Additionally, two identified proteins (carbonic anhydrase and protein disulfide isomerase) increased their concentration as provitamin D 3 became more abundant. Although our approach does not allow us to decrypt the functional relations between the proteinaceous and lipid components, nor under the semiochemical or struc- tural hypothesis, the finding that the proteins involved in this association were enzymes opens up to new perspectives about protein role: They may confer dynamic properties to the blend, making it able to compensate predictable variation of the envi- ronmental conditions. This may expand the view about proteins in the support-to-lipid hypothesis, from being a passive and inert component of the secretions to become an active and dynamic one, thus providing cues for future research.[IT] La comunicazione chimica nei vertebrati terrestri èspesso costituita da miscele complesse, in cui com- posti semiochimici e strutturali possono formare un“unitàfunzionaleintegrata. Nelle lucertole, molte specie hanno ghiandole epidermiche specializzate le cui secrezioni sono miscele cerose e omogenee di lipidi e proteine, entrambe attive nella comu- nicazione. L”intima coesistenza di tali composti lascia ipotizzare che essi debbano subire un certo grado di co-variazione, sia considerando il loro ruolo semiochimico, sia la funzione di supporto ai lipidi ipotizzata per la frazione proteica. Per valutare la presenza e il livello di covariazione proteine-lipidi, abbiamo confrontato la composizione e la complessitàdelle due frazioni nelle secrezioni della ghiandola femorale di 36 specie di lucertole, combinando l“analisi filogenetica comparativa con la spet- trometria di massa. Abbiamo riscontrato una forte correlazione tra la composizione e la complessitàdelle due frazioni. La composizione della frazione proteica èstata influenzata soprattutto dalla proporzione relativa di colestanolo, provitamina D 3 , stigmasterolo e tocoferolo, mentre la complessitàdelpattern proteico èaumentata con quella dei lipidi. Inoltre, due proteine identificate (anidrasi carbonica e disolfuro isomerasi) hanno aumentato la loro concentrazione al crescere dell’abbondanza della provitamina D 3 . Sebbene il nostro approccio non consenta di decifrare le relazioni funzionali tra le componenti proteiche e lipidiche, nésecondo l”ipotesi semiochimica nésecondo quella strutturale, la scoperta che le proteine coinvolte in questa asso- ciazione sono enzimi apre a nuove prospettive sul ruolo delle proteine stesse: esse potrebbero conferire proprietàdinamichealla miscela, rendendola capace di compensare le prevedibili variazioni delle condizioni ambientali. Questo puòampliare la visione delle proteine nell’ipotesi che esse siano di supporto ai lipidi, da componente passiva e inerte delle secrezioni a componente attiva e dinamica, fornendo cosìspunti per ricerche future.[ES] La comunicación química en los vertebrados terrestres se basa a menudo en mezclas complejas, donde los compuestos semioquímicos y estructurales pueden formar una unidad funcional integrada. En los lagartos y lagartijas, muchas especies tienen glándulas epidérmicas especializadas cuyas secreciones son mezclas cerosas y homogéneas de lípidos y proteínas, siendo ambos compuestos activos en la comunicación. La co-ocurrencia estrecha de tales compuestos permite plantear la hipótesis de que debería existir un cierto grado de covariación, considerando los posibles papeles de la fracción proteica tanto como semioquímicos y como apoyo a la función de los lípidos. Con el fin de evaluar la ocurrencia y el nivel de covariación entre proteínas y lípidos, comparamos la composición y complejidad de estas dos fracciones en las secreciones de la glándula femoral de 36 especies de lagartos y lagartijas, combinando análisis filogenéticos con espectrometría de masas en tándem. Encontramos que la composición y la complejidad de las dos fracciones estaban fuertemente correlacionadas. La com- posición de la fracción proteica estuvo influenciada principalmente por la proporción relativa de colestanol, provitamina D 3 , estigmasterol y tocoferol, mientras que la complejidad del patrón proteico aumentócon el de los líp idos. Además, dos proteínas identificadas (anhidrasa carbónica y proteína disulfuro isomerasa) aumentaban su concentración a medida que la provitamina D 3 era más abundante. Aunque nuestro enfoque no permite descifrar las relaciones funcionales entre los componentes pro- teináceos y lipídicos, ni bajo la hipótesis semioquímica, ni bajo la estructural, el hallazgo de que las proteínas involucradas en esta asociación serían enzimas abre nuevas perspectivas sobre el papel de las proteínas. Estas podrían conferir propiedades dinámicas a la mezcla, haciéndola capaz de compensar la variación esperada debida a las condiciones ambientales. Estos resul- tados pueden ampliar la visión del papel de las proteínas en la hipótesis de apoyo a los líp idos, pasando de ser un componente pasivo e inerte de las secreciones a convertirse en uno activo y dinámico, proporcionando asíideas para investigaciones futuras.M.M. was funded by Italian Ministry of University and Research, “Fondo Sociale Europeo REACT EU—Programma Operativo Nazionale Ricerca e Innovazione 2014–2020”. SB was funded by the Fonds Wetenschappelijk Onderzoek (FWO 12I8822N).Peer reviewe

Rapid and repeated divergence of animal chemical signals in an island introduction experiment

Studies of animal communication have documented myriad rapid, context-dependent changes in visual and acoustic signal design. In contrast, relatively little is known about the capacity of vertebrate chemical signals to rapidly respond, either plastically or deterministically, to changes in context. Four years following an experimental introduction of lizards to replicate experimental islets, we aimed to determine if chemical signal design of the experimental populations differed from that of the source population. In 2014, we translocated Podarcis erhardii lizards from a large, predator-rich island to each of five replicate predator-free islets. Mean population densities increased fivefold over the following 4 years and bite scars suggest significantly more intraspecific fighting among these experimental populations. In 2018, we analysed the chemical signal design of males in each of the experimental populations and compared it to the chemical signals of the source population. We found that males consistently presented a significantly more complex chemical signal compared to the source population. Moreover, their chemical signals were marked by high proportions of octadecanoic acid, oleic acid and α-tocopherol, the three compounds that are known to be associated with lizard territoriality and mate choice. Our island introduction experiment thus suggests that the chemical signal design of animals can shift rapidly and predictably in novel ecological contexts. © 2020 British Ecological Societ

Quantifying surface topography of biological systems from 3D scans

Understanding the three-dimensional (3D) surface complexity of biological systems can yield fundamental insights into how organisms interact with their environments. The wealth of current imaging technologies permits detailed 3D visualization of biological surfaces on the macro-, micro- and nanoscale. Analysis of the reconstructed 3D images, however, remains a challenging proposition. Here, we present QuSTo, a versatile, open-source program developed in Python to quantify surface topography from profiles obtained from 3D scans. The program calculates metrics that quantify surface roughness and the size (i.e. height and length) and shape (i.e. convexity constant (CC), skewness (S-k) and kurtosis (K-u)) of surface structures. We demonstrate the applicability of our program by quantifying the surface topography of snake skin based on newly collected data from white light 3D scans of the ventrum and dorsum of 32 species. To illustrate the utility of QuSTo for evolutionary and ecological research, we test whether snake species that occur in different habitats differ in skin surface structure using phylogenetic comparative analyses. The QuSTo application is free, open-source, user-friendly and easily adapted for specific analysis requirements (available in GitHub, github.com/GMLatUCDavis/QuSTo) and is compatible with 3D data obtained with different scanning techniques, for example, white light and laser scanning, photogrammetry, gel-based stereo-profilometry. Scientists from various disciplines can use QuSTo to examine the surface properties of an array of animal and plant species for both fundamental and applied biological and bioinspired research