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The evolution of tail weaponization in amniotes; Victoria M. Arbour, Lindsay E. Zanno Published 17 January 2018.DOI: 10.1098/rspb.2017.2299
Topic Started: Jan 18 2018, 11:28 AM (262 Views)
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Why don't turtles still have tail spikes?
Researchers explain why tail weaponry is rare


Date: January 17, 2018
Source: North Carolina State University
Summary:
In a study covering 300 million years of evolutionary history, researchers have found four necessary components to tail weapon development: size, armor, herbivory and thoracic stiffness.

We're all familiar with those awesome armored giants of the Jurassic and Cretaceous periods -- Stegosaurus and Ankylosaurus -- and their amazing, weaponized tails. But why aren't similar weaponized tails found in animals living today? In a study covering 300 million years of evolutionary history, researchers from North Carolina State University and the North Carolina Museum of Natural Sciences found four necessary components to tail weapon development: size, armor, herbivory and thoracic stiffness.

"Weapons like tail clubs and bony spikes are found only in a few extinct animals -- such as ankylosaurs, glyptodonts (large extinct armadillos) and in some ancient turtle species," says Victoria Arbour, former postdoctoral student at NC State, current postdoctoral fellow at the Royal Ontario Museum and corresponding author of a paper describing the research. "These same weapons just don't occur in modern-day animals, and we wanted to know why they were so rare even in the fossil record."

Study co-author Lindsay Zanno, professor of biological sciences at NC State and head of paleontology at the NC Museum of Natural Sciences, agrees, "We kicked off this study with a simple observation: most animal weapons used for combat are located on the most critical part of the body for survival, the head, as opposed to more expendable ones such as the tail. Why, we asked, wasn't evolution producing more animals with weaponized tails, when this would seem to be far less dangerous?"

To answer this question, Arbour and Zanno looked at a data set of 286 amniote species, both living and extinct, to see if there were patterns that pointed to the evolution of three specific types of tail weapons: bony spikes, a stiff tail or a bony knob at the tip of the tail. Amniotes refer to backboned, four-legged reptiles and mammals, as well as birds.

In the case of bony tail weaponry, the researchers found the animals had four things in common. First, they were usually large, weighing over 200 pounds (or 100 kilograms) -- about the weight of the glyptodonts that used to roam South America or a living mountain goat -- or were over three feet (a meter) long.

Second, armor was key. Ancient turtles, armadillos and armored dinosaurs were covered in some sort of hard carapace or bony plated armor. Thoracic stiffness -- referring to a body that doesn't bend side to side easily, perhaps so that it could easily counteract the forces needed to swing a large clubbed or spiked tail -- was also important. Finally, every animal in the fossil record that developed elaborate tail weaponry was an herbivore, or vegetarian.

"It's rare for large herbivores to have lots of bony armor to begin with," Arbour says, "and even rarer to see armored species with elaborate head or tail ornamentation because of the energy cost to the animal. The evolution of tail weaponry in Ankylosaurus and Stegosaurus required a 'perfect storm' of traits that aren't seen in living animals, and this unique combination explains why tail weaponry is rare even in the fossil record."

Zanno continues, "This study is an elegant example of how the fossil record can be used to better understand the world around us today."

Story Source: North Carolina State University. "Why don't turtles still have tail spikes? Researchers explain why tail weaponry is rare." ScienceDaily. www.sciencedaily.com/releases/2018/01/180117092338.htm (accessed January 17, 2018).




Journal Reference:
Victoria M. Arbour, Lindsay E. Zanno. The evolution of tail weaponization in amniotes. Proceedings of the Royal Society B: Biological Sciences, 2018; 285 (1871): 20172299 DOI: 10.1098/rspb.2017.2299

Abstract
Weaponry, for the purpose of intraspecific combat or predator defence, is one of the most widespread animal adaptations, yet the selective pressures and constraints governing its phenotypic diversity and skeletal regionalization are not well understood. Here, we investigate the evolution of tail weaponry in amniotes, a rare form of weaponry that nonetheless evolved independently among a broad spectrum of life including mammals, turtles and dinosaurs. Using phylogenetic comparative methods, we test for links between morphology, ecology and behaviour in extant amniotes known to use the tail as a weapon, and in extinct taxa bearing osseous tail armaments. We find robust ecological and morphological correlates of both tail lashing behaviour and bony tail weaponry, including large body size, body armour and herbivory, suggesting these life-history parameters factor into the evolution of antipredator behaviours and tail armaments. We suggest that the evolution of tail weaponry is rare because large, armoured herbivores are uncommon in extant terrestrial faunas, as they have been throughout evolutionary history.

1. Introduction
Weaponry is a common adaptation fundamental to understanding the evolutionary ecology of extant and extinct species [1,2]. Weapons may evolve via sexual selection, when males engage in intraspecific combat over reproductive resources [2,3], or through natural selection, as has been suggested for the horns of female bovids, which are used both as antipredator defences and in intraspecific combat for food resources [2,4]. They can also be co-opted from locomotor or feeding traits (e.g. talons, beaks or hooves [5]), or from defensive structures (e.g. spikes and quills [5]). Among extant amniotes, weapons are common in mammalian cervids and bovids, and are present in archosaurians and lepidosaurs (e.g. Anolis, agamids, chameleons and bucerotids) [2,6]. Differentiating weaponry from ornamentation or passive defences in extinct vertebrates is complicated by our inability to directly observe behaviours or empirically test for selective pressures. The strongest, most robust sexually selected structures are predicted to represent weaponry, whereas the most exaggerated and conspicuous structures are hypothesized to represent ornaments [3]. Bony structures inferred to be weapons are widespread in the fossil record, appearing in pareiasaurs, dicynodonts, rodents, artiodactyls, perissodactyls and non-avian dinosaurs [2].

The great phenotypic diversity of weapons in living species is known to be influenced by multiple factors including mating system, intensity of sexual selection, fighting style, body size and mechanical constraints [4,7–12]. However, rigorous studies attempting to define common ecological or anatomical correlates of weaponry within a broad phylogenetic framework are lacking and no research to our knowledge has attempted to study weaponry broadly in extinct vertebrates. Additionally, although the presence of amniote weaponry is phylogenetically widespread, its skeletal regionalization is not. The vast majority of weapons are modifications of the head or limbs, indicating that these areas undergo common selective pressures for weaponization despite the risks incurred by cranial combat [13–15]. By contrast, and although seemingly less risky, tail weaponization is exceptionally rare: bony tail weapons are found primarily in mammals, turtles and non-avian dinosaurs (figure 1; electronic supplementary material, S1), and tail lashing behaviour is found in lizards, crocodilians and mammals (figure 2; electronic supplementary material, S1). The rarity of tail armaments throughout amniote evolution, coupled with the rarity of use of the tail as a weapon in extant taxa, suggests that there may be anatomical or ecological constraints that prevented pervasive evolution of tail weaponry in amniotes.

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Figure 1. Phylogeny of Amniota showing the osteological traits associated with each independent origin of bony tail weaponry. Osteodermal elements are indicated in grey. Alternate tree topologies are figured in electronic supplementary material, S1. (Online version in colour.)

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Figure 2. Phylogeny of Amniota showing occurrences of observed use of the tail as a weapon. Interspecific or intraspecific tail lashing or whipping is present in aardvarks, porcupines, pangolins, multiple species of lizards and alligators. Although epidermal modifications such as keratinous spikes or quills may be present, bony tail spikes are only found in cordylid lizards. (Online version in colour.)

Here, we use phylogenetic comparative methods on extant phenotypic and paleontological datasets to identify the selective regime underlying the evolution of tail weaponization in amniotes. We note that many extinct taxa with tail weapons also share other unusual morphological adaptations, such as bony armour and distinct adaptations of the caudal vertebrae that serve to stiffen the tail [16]. Based on these observations and a survey of the life-history parameters of extant taxa known to use the tail as a weapon, we explore potential correlations between exaggerated tail armaments and a variety of morphological, ecological and behavioural traits within a predictive framework.

2. Material and methods
(a) Trait definition, choice and distribution
We consider the structures discussed in this paper to represent weaponry based on their robustness and previous biomechanical investigations of their functions [17–19], yet acknowledge they may have also functioned as ornaments; such a characterization would not change the significance of trait-to-trait correlation data we present here. We derived a dataset of binary traits hypothesized to be relevant to the evolution of tail weaponry (electronic supplementary material, S1 and S2), including detailed aspects of caudal anatomy, the morphology and distribution of armour, body mass, diet, locomotory mode and habitat. Predictions and rationales for including each of these traits are explained in detail in electronic supplementary material, S1.

Based on a review of taxa with putative tail weapons, we identify that osseous tail weaponry involves modifications to the stiffness of the distal tail, the mediolateral width of the tail terminus and the presence or absence of terminal tail spikes. Impressive bony tail clubs with stiff handles and enlarged distal tips are found in ankylosaurine dinosaurs and glyptodonts. Stegosaurid dinosaurs bear enlarged spikes at the tip of the tail that differ from the armour found elsewhere on the body, and both glyptodonts and meiolaniid turtles envelop the tail tip in dermal armour. Some early sauropod dinosaurs also expand the tip of a long, flexible tail. We therefore classify tail weaponry into two broad functional categories representing combinations of these three morphological traits: (i) tail clubs, which are formed via stiffening of at least the distal third of the tail and transverse expansion of the tail terminus; and (ii) tail flails, which remain flexible distally but bear armament at the terminus (e.g. bony spikes or transverse expansion).

(b) Tree topologies and branch lengths
We tested hypotheses on three tree topologies with 286 amniote taxa (grafted from published phylogenies) representing the current scope of uncertainty regarding the placement of turtles (electronic supplementary material, S3–S5). We created chronostratigraphically calibrated trees using the R paleotree v. 3.2.5 package [20] in RStudio v. 0.99.893 [21,22]. We calculated 100 trees for each tree topology using the timePaleoPhy function and the following parameters: minimum branch length scaling method (type = mbl), time variable set as 1 (vartime = 1), and time data as minimum and maximum bounds on a point date (dateTreatment = minMax). Trees were modified for publication using Figtree 1.4.2 [23] and Adobe Illustrator 15.1.0.

(c) Character correlation
We tested character correlations using pairwise comparisons in Mesquite v. 3.04 [24] and the Discrete module of BayesTraits v. 2.0 [25]. In Discrete, we ran maximum-likelihood analyses testing our full dataset against observed use of the tail as a weapon, a stiff distal tail, expanded distal tail tip or terminal bony spikes. We tested all trait combinations for significance using the omnibus test described by Pagel [26]. Trait pairs that were significant in the omnibus test were further investigated using the contingent change test [26] in BayesTraits (electronic supplementary material, S4).

We controlled for α-inflation from multiple comparisons by controlling the false discovery rate rather than the familywise error rate [27,28], using the method proposed by Benjamini & Hochburg [29] to determine significance levels for our correlations. Because correlation analyses such as Discrete can be susceptible to pseudoreplication [30], we also visually inspected the distribution of traits that were statistically significantly correlated; distributions representing unreplicated bursts or Darwin's scenario (sensu [30]) were not considered strong support for meaningful adaptive or functional links.

3. Results
(a) Traits correlated with tail lashing behaviour
Use of the tail as a weapon among extant taxa was correlated with the presence of spikes, osteoderms, thoracic armour, tail length, herbivory, a snout–vent length greater than 100 cm and a tail that is not prehensile (figure 3; electronic supplementary material, S7–S9). Most of these correlations were also recovered with at least one of the three bony tail weaponry traits we tested. The length of the tail was the only trait correlation unique to tail lashing behaviour. Tail lashing was more likely to evolve in the presence of osteoderms and spikes on the torso/pelvis, discontinuous armour in the thoracic region, a snout–vent length greater than 100 cm and herbivory (figure 4; electronic supplementary material, S10).

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Figure 3. Results of the correlation analyses, showing traits correlated with each of the three bony tail weapon traits (stiff distal tail, expanded tail tip and bony spikes), and traits correlated with any of these traits and tail lashing behaviour. (Online version in colour.)

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Figure 4. Results of the contingency analyses, showing which traits tail lashing behaviour and the three bony tail weapon traits are contingent upon.

(b) Traits correlated with bony tail weaponry
Several traits were correlated with all three bony tail weapon traits (figure 3; electronic supplementary material, S7–S9), including a stiff thoracic region, caudal osteoderms that envelop the tail tip and coossify with the distal caudal vertebrae, and anteriorly directed transverse processes on the anterior caudal vertebrae. Bony terminal tail spikes were correlated with coossified distal caudal vertebrae, a carapace with a central apex, osteoderms, spikes and armour on the torso, a wide pelvis, coossified haemal arches and caudal centra, and cranial weapons or ornaments, and weak support for a correlation with a stiff distal tail (figure 3; electronic supplementary material, S7–S9). An expanded tail tip was correlated with a stiff distal tail, expanded haemal arches that buttress the caudal centra, osteoderms forming a continuous tube around the distal caudals and body size greater than 100 kg and 500 kg (figure 3; electronic supplementary material, S7–S9). We additionally found weak support for correlations with herbivory, a wide pelvis and osteoderms on the torso. Stiffening of the distal tail was correlated with an expanded tail tip, tail spikes and osteoderms, coossified distal caudals, distal caudals that brace against the caudal osteoderms, a central carapace apex, spikes on the torso, coossified armour and a snout–vent length greater than 100 cm; it was negatively correlated with arboreality, posterolaterally oriented transverse processes, tail prehensility and bipedality (figure 3; electronic supplementary material, SI 7–9).

Evolving an expanded tail tip was contingent upon the presence of a stiff distal tail, buttressing haemal arches, and a stiff thoracic region, anterolaterally directed transverse processes, coossification of the caudal vertebrae and distal caudal osteoderms, and envelopment of the tail tip by caudal osteoderms (figure 4; electronic supplementary material, S10). Bony terminal tail spikes were contingent upon the presence of a stiff thoracic region, osteoderms and spikes on the torso, envelopment of the tail tip by caudal osteoderms, anterolaterally directed transverse processes, and caudals that brace against the osteoderms (figure 4; electronic supplementary material, S10). Evolving a stiff distal tail was not contingent on the state of any traits in our dataset (figure 4; electronic supplementary material, S10).

4. Discussion
Amniote tails are rarely invoked as antipredator defences or in intraspecific combat (figure 2). New and Old World porcupines [31,32], pangolins [33,34], aardvarks [35], and lizards such as Iguana iguana [36], Ctenosaura [37], Smaug giganteus [38], Uromastyx aegiptius [37] and some varanids [39] are known to use the tail as a weapon, typically as an antipredator defence. Agama agama is one of the only examples of an extant amniote that uses its tail as a weapon in male–male combat [40]. Only one anatomical trait specific to the tail (its length) was correlated with tail lashing, suggesting that this behaviour can evolve in animals with tails of various morphologies. No extant amniotes are proposed to bear sexually selected bony tail weapons, and to our knowledge spiked tails on extant taxa have not been interpreted as the products of selection for intraspecific combat. Only Smaug has bony spikes on the tail, and these are not elaborated to the degree seen in extinct taxa. Varanus komodoensis has small osteoderms that do not form spikes; porcupines, pangolins and Uromastyx have spikes composed exclusively of keratin; and Agama, Iguana and Orycteropus lack spikes or osteoderms entirely.

Tail lashing is most likely to be present in medium- or large-sized, armoured, spiky herbivores. In mammals, defensive armour is more likely to evolve in species that are neither small enough to render crypsis effective nor large enough for body size to deter predators, and which live in relatively open habitats and/or forage in such a way that they cannot remain vigilant [41]. In lizards, tail lashing is also commonly encountered in species that retreat into rock crevices to avoid predators, such as Uromastyx and Smaug [37]. Using the tail as a weapon appears to be a strategy of last resort for many taxa and is only employed after crypsis, vigilance, speed or escape into a refuge have failed. As such, the selective pressures favouring the evolution of this behaviour may be weaker than for other antipredator strategies, especially given that direct combat with a predator is risky, which may explain why tail lashing is a rarely observed behaviour among extant amniotes.

The results from our comparative analyses indicate that the evolution of bony tail weaponry is subject to a series of wide-ranging morphological and ecological constraints that might limit its repeated appearance in amniote evolution (figures 3 and 4). Bony tail weaponry is predicated on a specific suite of traits including large body size, body armour (in the form of carapaces, osteoderms or spikes), thoracic stiffness and herbivory. Although present in a variety of extinct taxa, this combination of features is largely absent in the majority of living species, which may explain why there are no tail clubs or tail flails observed in extant amniotes that use the tail as a weapon. For example, the largest extant cingulate, Priodontes maximus, does not exceed the body size thresholds correlated with tail weaponry, and the largest extant amniotes bearing osteoderms or spikes—Dermochelys coriacea and crocodilians—are aquatic and carnivorous. Amniotes that use the tail for locomotion (e.g. arboreal species with prehensile tails) are unlikely to use the tail as a weapon or to have evolved tail weaponry. We suggest that the rarity of bony tail weaponry in extant amniotes reflects that there are few extant large-bodied herbivores bearing bony armour.

Both bony tail weaponry and tail lashing behaviour were correlated with the presence of thoracic armour, either in the form of epidermal spikes, osteoderms or a carapace, and in some cases the evolution of tail weaponry was contingent on the presence of thoracic armour. As such, tail weaponry is probably partly constrained by the selective pressures underlying the evolution of armour more generally. Although cranial weapons often evolve via sexual selection [2], body armour is typically thought to have evolved as a defence against predation, but the parameters underlying its evolution in some species and not others are complex and as yet poorly understood. Experimental studies of stickleback indicate that body armour evolves in response to increasing predation pressure, especially from gape-limited predators [42–44]. In cordylid lizards, armour confers protection against predation [45], yet limits escape speed [46], and its relative development in different species may reflect thermal habitat partitioning [47]. Armour appears to evolve in intermediately sized insectivorous mammals living in open habitats, which are unable to use large body size, crypsis or vigilance to avoid predation [41,48,49]

Our data also bear on functional precursors necessary for bony tail weaponry to evolve. We found a significant correlation between thoracic rigidity and the evolution of a tail club, despite using conservative parameters to define rigidity. Tschopp & Mateus [50] suggested that increased rigidity in the pectoral girdle of some sauropods may have functioned as a brace against lateral tail movements, and noted a possible correlation between trunk rigidity and tail weaponry in sauropods. Although our dataset did not address the rigidity of the pectoral girdle, our results indicate that general thoracic stiffness may be important for the evolution of tail weaponry in amniotes. We also recovered a variety of traits linked to functional stiffening of the tail to be necessarily present prior to the evolution of bony expansions or spikes on the tail terminus in extinct amniotes, although the selective regime favouring a stiff distal tail remains unclear.

Our data suggest that adaptive responses to predation pressure were necessary precursors to the evolution of bony tail weapons. Tail lashing behaviour in extant amniotes is almost always an antipredator defence strategy (electronic supplementary material, S1). The tail clubs of ankylosaurs and glyptodonts were morphologically complex, physiologically costly, possibly positively allometric and taxonomically variable [51], and as such may have been sexually selected weapons [52]. Our correlations suggest that bony tail weaponry may have evolved in some taxa that co-opted tail lashing and body armour as antipredation strategies for use in intraspecific combat, resulting in the evolution of elaborate tail clubs or flails. In such a scenario, bony tail weaponry results from iterative selective pressures beginning with passive predator deterrence (general body armour), to active predator deterrence (tail lashing) and possibly to conspecific combat (tail clubs and flails). We find that the rarity of bony tail weaponry thus probably reflects the idiosyncratic nature of tail lashing as a behavioural strategy, combined with the constraints surrounding the evolution of large body size, thoracic stiffness and armour.


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