How seasonality influences the thermal biology of lizards with different thermoregulatory strategies: a meta-analysis.

Ectotherms that maintain thermal balance in the face of varying climates should be able to colonise a wide range of habitats. In lizards, thermoregulation usually appears as a variety of behaviours that buffer external influences over physiology. Basking species rely on solar radiation to raise body temperatures and usually show high thermoregulatory precision. By contrast, species that do not bask are often constrained by climatic conditions in their habitats, thus having lower thermoregulatory precision. While much focus has been given to the effects of mean habitat temperatures, relatively less is known about how seasonality affects the thermal biology of lizards on a macroecological scale. Considering the current climate crisis, assessing how lizards cope with temporal variations in environmental temperature is essential to understand better how these organisms will fare under climate change. Activity body temperatures (Tb ) represent the internal temperature of an animal measured in nature during its active period (i.e. realised thermal niche), and preferred body temperatures (Tpref ) are those selected by an animal in a laboratory thermal gradient that lacks thermoregulatory costs (i.e. fundamental thermal niche). Both traits form the bulk of thermal ecology research and are often studied in the context of seasonality. In this study, we used a meta-analysis to test how environmental temperature seasonality influences the seasonal variation in the Tb and Tpref of lizards that differ in thermoregulatory strategy (basking versus non-basking). Based on 333 effect sizes from 137 species, we found that Tb varied over a greater magnitude than Tpref across seasons. Variations in Tb were not influenced by environmental temperature seasonality; however, body size and thermoregulatory strategy mediated Tb responses. Specifically, larger species were subjected to greater seasonal variations in Tb , and basking species endured greater seasonal variations in Tb compared to non-basking species. On the other hand, the seasonal variation in Tpref increased with environmental temperature seasonality regardless of body size. Thermoregulatory strategy also influenced Tpref , suggesting that behaviour has an important role in mediating Tpref responses to seasonal variations in the thermal landscape. After controlling for phylogenetic effects, we showed that Tb and Tpref varied significantly across lizard families. Taken together, our results support the notion that the relationship between thermal biology responses and climatic parameters can be taxon and trait dependent. Our results also showcase the importance of considering ecological and behavioural aspects in macroecological studies. We further highlight current systematic, geographical, and knowledge gaps in thermal ecology research. Our work should benefit those who aim to understand more fully how seasonality shapes thermal biology in lizards, ultimately contributing to the goal of elucidating the evolution of temperature-sensitive traits in ectotherms.

Wettability and morphology of proboscises interweave with hawkmoth evolutionary history.

Hovering hawkmoths expend significant energy while feeding, which should select for greater feeding efficiency. Although increased feeding efficiency has been implicitly assumed, it has never been assessed. We hypothesized that hawkmoths have proboscises specialized for gathering nectar passively. Using contact angle and capillary pressure to evaluate capillary action of the proboscis, we conducted a comparative analysis of wetting and absorption properties for 13 species of hawkmoths. We showed that all 13 species have a hydrophilic proboscis. In contradistinction, the proboscises of all other tested lepidopteran species have a wetting dichotomy with only the distal ∼10% hydrophilic. Longer proboscises are more wettable, suggesting that species of hawkmoths with long proboscises are more efficient at acquiring nectar by the proboscis surface than are species with shorter proboscises. All hawkmoth species also show strong capillary pressure, which, together with the feeding behaviors we observed, ensures that nectar will be delivered to the food canal efficiently. The patterns we found suggest that different subfamilies of hawkmoths use different feeding strategies. Our comparative approach reveals that hawkmoths are unique among Lepidoptera and highlights the importance of considering the physical characteristics of the proboscis to understand the evolution and diversification of hawkmoths.

Haemolymph viscosity in hawkmoths and its implications for hovering flight.

Viscosity determines the resistance of haemolymph flow through the insect body. For flying insects, viscosity is a major physiological parameter limiting flight performance by controlling the flow rate of fuel to the flight muscles, circulating nutrients and rapidly removing metabolic waste products. The more viscous the haemolymph, the greater the metabolic energy needed to pump it through confined spaces. By employing magnetic rotational spectroscopy with nickel nanorods, we showed that viscosity of haemolymph in resting hawkmoths (Sphingidae) depends on wing size non-monotonically. Viscosity increases for small hawkmoths with high wingbeat frequencies, reaches a maximum for middle-sized hawkmoths with moderate wingbeat frequencies, and decreases in large hawkmoths with slower wingbeat frequencies but greater lift. Accordingly, hawkmoths with small and large wings have viscosities approaching that of water, whereas hawkmoths with mid-sized wings have more than twofold greater viscosity. The metabolic demands of flight correlate with significant changes in circulatory strategies via modulation of haemolymph viscosity. Thus, the evolution of hovering flight would require fine-tuned viscosity adjustments to balance the need for the haemolymph to carry more fuel to the flight muscles while decreasing the viscous dissipation associated with its circulation.

The hidden links between animal weapons, fighting style, and their effect on contest success: a meta-analysis.

In many species that fight over resources, individuals use specialized structures to gain a mechanical advantage over their rivals during contests (i.e. weapons). Although weapons are widespread across animals, how they affect the probability of winning contests is still debated. According to theory, understanding weapon function during contests is essential to: (i) understanding its importance in determining the winner, and (ii) identifying what weapon traits (e.g. weapon length versus shape versus performance) are most relevant for contest success. However, quantitative evaluations of how weapon function affects the extent to which weapon traits influence contest success are still lacking. Here, we first develop an individual-based model to evaluate how increasing the influence of the weapon in determining the winner translates to differences between winners and losers. Then, we use a meta-analysis to identify: (i) whether different weapon measures influence contest outcome differently; (ii) how animals use their weapons during fights - i.e. weapon function; and (iii) if weapon function correlates to how weapons influence contest outcome. Our model showed that, as weapons increased the chance of determining the winner, the mean difference between winners and losers also increased. Therefore, in our meta-analysis we used the mean trait difference between winners and losers as a proxy for the extent to which weapons influence contest success. The literature search identified 49 suitable studies, containing information for 52 species, totalling 107 effect sizes. Four main patterns emerged. First, most of the literature focuses on linear measures of weapons, while performance measures are concentrated on Crustacea and Squamata; other types of measures were rare. Second, differences between winners and losers in linear measurements were greater than differences in performance measurements when all species were combined (and when we used only a subset). Third, species that bear weapons almost always perform visual/tactile displays before engaging in physical contact. And fourth, while the way individuals display their weapons did not influence the importance of weapon size on contest outcomes, fighting style predicted when differences between winners and losers would be higher. Species that used their weapons to push or lift (even when combined with other functions) showed greater differences between winners and losers when compared to species that used their weapons to impact, pierce, pull or squeeze. Overall, our results show that we have an incomplete understanding of animal weapons built mostly on weapon size and a few select taxa. Thus, we should start focusing on measuring weapons according to how they are used during contests and in a wider diversity of species. One way forward is to conduct studies that integrate weapon morphology to weapon function to ensure we are measuring the most ecologically relevant variables.

Flight hampers the evolution of weapons in birds.

Birds are a remarkable example of how sexual selection can produce diverse ornaments and behaviours. Specialised fighting structures like deer's antlers, in contrast, are mostly absent among birds. Here, we investigated if the birds' costly mode of locomotion-powered flight-helps explain the scarcity of weapons among members of this clade. Our simulations of flight energetics predicted that the cost of bony spurs-a specialised avian weapon-should increase with time spent flying. Bayesian phylogenetic comparative analyses using a global spur dataset corroborated this prediction. First, extant species with flight-efficient wings (which presumably fly more frequently) tend to have fewer or no bony spurs. Second, this association likely arose because flying more leads to more frequent evolutionary loss of spurs. Together, these findings suggest that, much like pneumatic bones, absence of weaponry may be another feature of the avian body plan that allows birds to efficiently explore the aerial habitat.

Biomechanics influence sexual dimorphism in the giant mesquite bug, Thasus neocalifornicus.

In many species, males possess specialized weaponry that confers benefits during male-male combat. Because male weapons are often disproportionately larger versions of preexisting body parts, females often possess reduced versions of male weaponry. Most research focuses exclusively on sexual dimorphism in the size of male and female weapons, even though other aspects such as weapon performance can also explain the evolution of weapon sexual dimorphism. In the giant mesquite bug, Thasus neocalifornicus, males wield exaggerated hindlegs that aid in locomotion and are used as weapons to generate forceful squeezes during combat. However, female T. neocalifornicus hindlegs are relatively inconspicuous and only used for locomotion. To understand the intricacies of weapon sexual dimorphism in T. neocalifornicus hindlegs, we measured the allometry of their hindlegs morphology, biomechanics, and performance. Males and females had relatively similar sized legs when concerning only linear measurements: hindleg length did not differ between the sexes (both for intercept and slope), but males do have relatively wider hindlegs (greater intercepts). Regarding performance, however, males were relatively and proportionally stronger than females. Furthermore, the output lever of male hindlegs scales hypoallometrically and the tibial spine maintains its position as the hindlegs grows, both of which maintain the hindlegs' biomechanical efficiency as they increase in size. Overall, our finding demonstrates that selection on the performance and biomechanics of sexually selected weapons can influence the expression of sexual dimorphism, by exaggerating some aspects of the weapons morphology-but constraining others.

Supergroup F Wolbachia in terrestrial isopods: Horizontal transmission from termites?

Horizontal transmission between distantly related species has been used to explain how Wolbachia infect multiple species at astonishing rates despite the selection for resistance. Recently, a terrestrial isopod species was found to be infected by an unusual strain of supergroup F Wolbachia. However, only Wolbachia of supergroup B is typically found in isopods. One possibility is that these isopods acquired the infection because of their recurrent contact with termites-a group with strong evidence of infection by supergroup F Wolbachia. Thus, our goals were: (1) check if the infection was an isolated case in isopods, or if it revealed a broader pattern; (2) search for Wolbachia infection in the termites within Brazil; and (3) look for evidence consistent with horizontal transmission between isopods and termites. We collected Neotroponiscus terrestrial isopods and termites along the Brazilian coastal Atlantic forest. We sequenced and identified the Wolbachia strains found in these groups using coxA, dnaA, and fpbA genes. We constructed phylogenies for both bacteria and host taxa and tested for coevolution. We found the supergroup F Wolbachia in other species and populations of Neotroponiscus, and also in Nasutitermes and Procornitermes termites. The phylogenies showed that, despite the phylogenetic distance between isopods and termites, the Wolbachia strains clustered together. Furthermore, cophylogenetic analyses showed significant jumps of Wolbachia between terrestrial isopods and termites. Thus, our study suggests that the horizontal transmission of supergroup F Wolbachia between termites and terrestrial isopods is likely. Our study also helps understanding the success and worldwide distribution of this symbiont. SUPPLEMENTARY INFORMATION: The online version of this article (10.1007/s10682-021-10101-4) contains supplementary material, which is available to authorized users.

Harder, better, faster, stronger: Weapon size is more sexually dimorphic than weapon biomechanical components in two freshwater anomuran species.

Sexual selection influences the evolution of morphological traits that increase the likelihood of monopolizing scarce resources. When such traits are used during contests, they are termed weapons. Given that resources are typically linked to monopolizing mating partners, theory expects only males to bear weapons. In some species, however, females also bear weapons, although typically smaller than male weapons. Understanding why females bear smaller weapons can thus help us understand the selective pressures behind weapon evolution. However, most of our knowledge comes from studies on weapon size, while the biomechanics of weapons, such as the size of the muscles, efficiency, and shape are seldom studied. Our goal was to test if the theoretical expectations for weapon size sexual dimorphism also occur for weapon biomechanics using two aeglid crab species. Males of both species had larger claws which were also stronger than female claws. Male claws were also more efficient than females' claws (although we used only one species in this analysis). For weapon shape, though, only one species differed in the mean claw shape. Regarding scaling differences, in both species, male claws had higher size scaling than females, while only one species had a higher shape scaling. However, male weapons did not have higher scaling regarding strength and efficiency than females. Thus, males apparently allocate more resources in weapons than females, but once allocated, muscle and efficiency follow a similar developmental pathway in both sexes. Taken together, our results show that sexual dimorphism in weapons involves more than differences in size. Shape differences are especially intriguing because we cannot fully understand its causes. Yet, we highlight that such subtle differences can only be detected by measuring and analysing weapon shape and biomechanical components. Only then we might better understand how weapons are forged.

The longer the better: evidence that narwhal tusks are sexually selected.

Once thought to be the magical horn of a unicorn, narwhal tusks are one of the most charismatic structures in biology. Despite years of speculation, little is known about the tusk's function, because narwhals spend most of their lives hidden underneath the Arctic ice. Some hypotheses propose that the tusk has sexual functions as a weapon or as a signal. By contrast, other hypotheses propose that the tusk functions as an environmental sensor. Since assessing the tusks function in nature is difficult, we can use the morphological relationships of tusk size with body size to understand this mysterious trait. To do so, we collected morphology data on 245 adult male narwhals over the course of 35 years. Based on the disproportional growth and large variation in tusk length we found, we provide the best evidence to date that narwhal tusks are indeed sexually selected. By combining our results on tusk scaling with known material properties of the tusk, we suggest that the narwhal tusk is a sexually selected signal that is used during male-male contests.

Underwater compensation for exaggerated weaponry: The role of morphology and environment on crab locomotor performance.

Exaggerated morphologies may increase fitness, but they might be costly to bear; heavy weight, for instance, might hinder locomotion. Evidence supporting these costs are sparse because animals that move on land or swim have traits reducing those costs, called compensatory traits. Animals that walk underwater, however, are under different environmental pressures than land animals. Buoyancy, for instance, reduces the effective weight of any object, which could decrease the locomotion costs of carrying exagerrated traits. Hence, underwater species might maintain performance without compensation. To test this, we compared males of the freshwater anomuran Aegla longirostri that bear an exaggerated claw to females (the natural control). We first tested whether the exaggerated claw decreased male locomotor performance. Next, we tested if sexual dimorphism in performance is associated with differences in leg asymmetry, length, and muscle size. Lastly, we tested if large males have proportionally heavier legs than smaller males. Unexpectedly, females are faster than males while also having relatively longer legs than males. Therefore, females might walk faster because of the longer legs, which might be unrelated to the male exaggerated claw. Furthermore, larger males did not have proportionally heavier legs than smaller males, further suggesting no compensation. Hence, even though aeglid's claw weigh ~25% of their total body weight, we did not find evidence for burden or compensation on males. The environment might thus decrease the costs of exaggerated traits.

All by myself? Meta-analysis of animal contests shows stronger support for self than for mutual assessment models.

Since the 1970's, models based on evolutionary game theory, such as war of attrition (WOA), energetic war of attrition (E-WOA), cumulative assessment model (CAM) and sequential assessment model (SAM), have been widely applied to understand how animals settle contests. Despite the important theoretical advances provided by these models, empirical evidence indicates that rules adopted by animals to settle contests vary among species. This stimulated recent discussions about the generality and applicability of models of contest. A meta-analysis may be helpful to answer questions such as: (i) is there a common contest rule to settle contests; (ii) do contest characteristics, such as the occurrence of physical contact during the fight, influence the use of specific contest rules; and (iii) is there a phylogenetic signal behind contest rules? To answer these questions, we gathered information on the relationship between contest duration and traits linked to contestants' resource holding potential (RHP) for randomly paired rivals and RHP-matched rivals. We also gathered behavioural data about contest escalation and RHP asymmetry. In contests between randomly paired rivals, we found a positive relationship between contest duration and loser RHP but did not find any pattern for winners. We also found a low phylogenetic signal and a similar response for species that fight with and without physical contact. In RHP-matched rivals, we found a positive relationship between contest duration and the mean RHP of the pair. Finally, we found a negative relation between contest escalation and RHP asymmetry, even though it was more variable than the other results. Our results thus indicate that rivals settle contests following the rules predicted by WOA and E-WOA in most species. However, we also found inconsistencies between the behaviours exhibited during contests and the assumptions of WOA models in most species. We discuss additional (and relatively untested) theoretical possibilities that may be explored to resolve the existing inconsistencies.

How does environment influence fighting? The effects of tidal flow on resource value and fighting costs in sea anemones.

An animal's decision to enter into a fight depends on the interaction between perceived resource value (V) and fighting costs (C). Both could be altered by predictable environmental fluctuations. For intertidal marine animals, such as the sea anemone Actinia equina, exposure to high flow during the tidal cycle may increase V by bringing more food. It may also increase C via energy expenditure needed to attach to the substrate. We asked whether simulated tidal cycles would alter decisions in fighting A. equina We exposed some individuals to still water and others to simulated tidal cycles. To gain insights into V, we measured their startle responses before and after exposure to the treatments, before staging dyadic fights. Individuals exposed to flow present shorter startle responses, suggesting that flowing water indicates high V compared with still water. A higher probability of winning against no-flow individuals and longer contests between flow individuals suggests that increased V increases persistence. However, encounters between flow individuals were less likely to escalate, suggesting that C is not directly related to V. Therefore, predictable environmental cycles alter V and C, but in complex ways.