Revisiting the cost of carnivory in mammals.

Predator-prey relationships play a key role in the evolution and ecology of carnivores. An understanding of predator-prey relationships and how this differs across species and environments provides information on how carnivorous strategies have evolved and how they may change in response to environmental change. We aim to determine how mammals overcame the challenges of living within the marine environment; specifically, how this altered predator-prey body mass relationships relative to terrestrial mammals. Using predator and prey mass data collected from the literature, we applied phylogenetic piecewise regressions to investigate the relationship between predator and prey size across carnivorous mammals (51 terrestrial and 56 marine mammals). We demonstrate that carnivorous mammals have four broad dietary groups: small marine carnivores (< 11 000 kg) and small terrestrial carnivores (< 11 kg) feed on prey less than 5 kg and 2 kg, respectively. On average, large marine carnivores (> 11 000 kg) feed on prey equal to 0.01% of the carnivore's body size, compared to 45% or greater in large terrestrial carnivores (> 11 kg). We propose that differences in prey availability, and the relative ease of processing large prey in the terrestrial environment and small prey in marine environment, have led to the evolution of these novel foraging behaviours. Our results provide important insights into the selection pressures that may have been faced by early marine mammals and ultimately led to the evolution of a range of feeding strategies and predatory behaviours.

Ornament size and colour as alternative strategies for effective communication in gliding lizards.

Sexual ornamentation needs to be conspicuous to be effective in attracting potential mates and defending territories and indeed, a multitude of ways exists to achieve this. Two principal mechanisms for increasing conspicuousness are to increase the ornament's colour or brightness contrast against the background and to increase the size of the ornament. We assessed the relationship between the colour and size of the dewlap, a large extendible throat-fan, across a range of species of gliding lizards (Agamidae; genus Draco) from Malaysia and the Philippines. We found a negative relationship across species between colour contrast against the background and dewlap size in males, but not in females, suggesting that males of different species use increasing colour contrast and dewlap size as alternative strategies for effective communication. Male dewlap size also increases with increasing sexual size dimorphism, and dewlap colour and brightness contrast increase with increasing sexual dichromatism in colour and brightness, respectively, suggesting that sexual selection may act on both dewlap size and colour. We further found evidence that relative predation intensity, as measured from predator attacks on models placed in the field, may play a role in the choice of strategy (high chromatic contrast or large dewlap area) a species employs. More broadly, these results highlight that each component in a signal (such as colour or size) may be influenced by different selection pressures and that by assessing components individually, we can gain a greater understanding of the evolution of signal diversity.

Repeated evolution of exaggerated dewlaps and other throat morphology in lizards.

The existence of elaborate ornamental structures in males is often assumed to reflect the outcome of female mate choice for showy males. However, female mate choice appears weak in many iguanian lizards, but males still exhibit an array of ornament-like structures around the throat. We performed a phylogenetic comparative study to assess whether these structures have originated in response to male-male competition or the need for improved signal efficiency in visually difficult environments. We found little evidence for the influence of male-male competition. Instead, forest species were more likely to exhibit colourful throat appendages than species living in open habitats, suggesting selection for signal efficiency. On at least three independent occasions, throat ornamentation has become further elaborated into a large, conspicuously coloured moving dewlap. Although the function of the dewlap is convergent, the underlying hyoid apparatus has evolved very differently, revealing the same adaptive outcome has been achieved through multiple evolutionary trajectories. More generally, our findings highlight that extravagant, ornament-like morphology can evolve in males without the direct influence of female mate choice and that failure to consider alternative hypotheses for the evolution of these structures can obscure the true origins of signal diversity among closely related taxa.

Marked colour divergence in the gliding membranes of a tropical lizard mirrors population differences in the colour of falling leaves.

Populations of the Bornean gliding lizard, Draco cornutus, differ markedly in the colour of their gliding membranes. They also differ in local vegetation type (mangrove forest versus lowland rainforest) and consequently, the colour of falling leaves (red and brown/black in mangrove versus green, brown and black in rainforest). We show that the gliding membranes of these lizards closely match the colours of freshly fallen leaves in the local habitat as they appear to the visual system of birds (their probable predators). Furthermore, gliding membranes more closely resembled colours of local fallen leaves than standing foliage or fallen leaves in the other population's habitat. This suggests that the two populations have diverged in gliding membrane coloration to match the colours of their local falling leaves, and that mimicking falling leaves is an adaptation that functions to reduce predation by birds.

Key innovations and island colonization as engines of evolutionary diversification: a comparative test with the Australasian diplodactyloid geckos.

The acquisition of key innovations and the invasion of new areas constitute two major processes that facilitate ecological opportunity and subsequent evolutionary diversification. Using a major lizard radiation as a model, the Australasian diplodactyloid geckos, we explored the effects of two key innovations (adhesive toepads and a snake-like phenotype) and the invasion of new environments (island colonization) in promoting the evolution of phenotypic and species diversity. We found no evidence that toepads had significantly increased evolutionary diversification, which challenges the common assumption that the evolution of toepads has been responsible for the extensive radiation of geckos. In contrast, a snakelike phenotype was associated with increased rates of body size evolution and, to a lesser extent, species diversification. However, the clearest impact on evolutionary diversification has been the colonization of New Zealand and New Caledonia, which were associated with increased rates of both body size evolution and species diversification. This highlights that colonizing new environments can drive adaptive diversification in conjunction or independently of the evolution of a key innovation. Studies wishing to confirm the putative link between a key innovation and subsequent evolutionary diversification must therefore show that it has been the acquisition of an innovation specifically, not the colonization of new areas more generally, that has prompted diversification.

Historical contingency and behavioural divergence in territorial Anolis lizards.

The extent that evolution - including adaptation - is historically contingent (dependent on past events) has often been hotly debated, but is still poorly understood. In particular, there are little data on the degree that behaviour, an aspect of the phenotype that is strongly linked to contemporary environments (social or physical), retains the imprint of evolutionary history. In this study, I examined whether differences in the design of the territorial displays among species of Caribbean Anolis lizards reflect island-specific selection regimes, or historically contingent predispositions associated with different clade histories. Adult males advertise territory ownership using a series of headbobs and dewlap extensions, bouts of which vary in duration among species. When display durations were mapped onto the Anolis phylogeny, prominent differences between species belonging to the Western and Eastern Caribbean radiations were apparent. Statistical analyses confirmed that species differences in the duration of headbob displays, and to some extent the duration of dewlap extensions, were historically contingent. The unique evolutionary histories of each clade have seemingly had a profound effect on the subsequent direction of display evolution among descendent taxa. These results combined with those from previous studies on these lizards show that past history can have an important impact on the type of behaviour exhibited by species today, to the point that adaptive evolution can proceed quite differently in lineages originating from different evolutionary starting points.

Fossils and phylogeny uncover the evolutionary history of a unique antipredator behaviour.

Recently, two squirrel species (Spermophilus spp.) were discovered to anoint their bodies with rattlesnake scent as a means of concealing their odour from these chemosensory predators. In this study, we tested multiple species with predator scents (rattlesnake and weasel) to determine the prevalence of scent application across the squirrel phylogeny. We reconstructed the evolutionary history of the behaviour using a phylogenetic analysis and fossil records of historic predator co-occurrence. Squirrels with historical and current rattlesnake co-occurrence all applied rattlesnake scent, whereas no relationship existed between weasel scent application and either weasel or rattlesnake co-occurrence. This was surprising because experimental tests confirmed rattlesnake and weasel scent were both effective at masking prey odour from hunting rattlesnakes (the primary predator of squirrels). Ancestral reconstructions and fossil data suggest predator scent application in squirrels is ancient in origin, arising before co-occurrences with rattlesnakes or weasels in response to some other, now extinct, chemosensory predator.

Ornament evolution in dragon lizards: multiple gains and widespread losses reveal a complex history of evolutionary change.

The expression in females of ornaments thought to be the target of sexual selection in males is a long-standing puzzle. Two main hypotheses are proposed to account for the existence of conspicuous ornaments in both sexes (mutual ornamentation): genetic correlation between the sexes and sexual selection on females as well as males. We examined the pattern of ornament gains and losses in 240 species of dragon lizards (Agamidae) in order to elucidate the relative contribution of these two factors in the evolution of mutual ornamentation. In addition, we tested whether the type of shelter used by lizards to avoid predators predicts the evolutionary loss or constraint of ornament expression. We found evidence that the origin of female ornaments is broadly consistent with the predictions of the genetic correlation hypothesis. Ornaments appear congruently in both sexes with some lineages subsequently evolving male biased sexual dimorphism, apparently through the process of natural selection for reduced ornamentation in females. Nevertheless, ornaments have also frequently evolved in both sexes independently. This suggests that genetic correlations are potentially weak for several lineages and sexual selection on females is responsible for at least some evolutionary change in this group. Unexpectedly, we found that the evolutionary loss of some ornaments is concentrated more in males than females and this trend cannot be fully explained by our measures of natural selection.

Individual, sexual, seasonal, and temporal variation in the amount of sagebrush lizard scent marks.

Although many animals deposit scent marks, previous studies have focused almost entirely on rodents or on the chemical structure of the signal. Here, we study the quantity and temporal pattern of chemical deposition by the territorial sagebrush lizard Sceloporus graciosus, measuring both femoral pore and fecal deposits. Specifically, we tested whether variation in deposition is a good cue of individual and sexual identity and/or whether it is more closely associated with body size and reproductive state, indicators of physiological condition. The results support the latter hypothesis. We found that although the amount of fluid deposited on a single perch (rarely quantified in mammals) carries little information on individual or sexual identity, it reflects the physiological condition and reproductive state of individual lizards and is replenished on a roughly weekly cycle, potentially providing additional information on the producer's activity level. The amount of deposition may thus provide important information to chemical receivers making mate choice and territorial defense decisions. The results further suggest that seasonal increases in gland production allow lizards to mark more sites rather than to influence the quality of the signal on a single perch.

Intrasexual selection predicts the evolution of signal complexity in lizards.

Sexual selection has often been invoked in explaining extravagant morphological and behavioural adaptations that function to increase mating success. Much is known about the effects of intersexual selection, which operates through female mate choice, in shaping animal signals. The role of intrasexual selection has been less clear. We report on the first evidence for the coevolution of signal complexity and sexual size dimorphism (SSD), which is characteristically produced by high levels of male male competition. We used two complementary comparative methods in order to reveal that the use of complex signals is associated with SSD in extant species and that historical increases in complexity have occurred in regions of a phylogenetic tree characterized by high levels of pre-existing size dimorphism. We suggest that signal complexity has evolved in order to improve opponent assessment under conditions of high male male competition. Our findings suggest that intrasexual selection may play an important and previously underestimated role in the evolution of communicative systems.