Evolutionary loss of complexity in animal signals: cause and consequence.

We identified hypotheses for the cause and consequences of the loss of complexity in animal signals and tested these using a genus of visually communicating lizards, the Southeast Asian Draco lizards. Males of some species have lost the headbob component from their display, which is otherwise central to the communication of this genus. These males instead display a large, colorful dewlap to defend territories and attract mates. This dewlap initially evolved to augment the headbob component of the display, but has become the exclusive system of communication. We tested whether the loss of headbobs was caused by relaxed selection, habitat-dependent constraints, or size-specific energetic constraints on display movement. We then examined whether the consequences of this loss have been mitigated by increased signaling effort or complexity in the color of the dewlap. It appears the increased cost of display movement resulting from the evolution of large body size might have contributed to the loss of headbobs and has been somewhat compensated for by the evolution of greater complexity in dewlap color. However, this evolutionary shift is unlikely to have maintained the complexity previously present in the communication system, resulting in an apparent detrimental loss of information potential.

Global effects of forest modification on herpetofauna communities.

As the area covered by human-modified environments grows, it is increasingly important to understand the responses of communities to the novel habitats created, especially for sensitive and threatened taxa. We aimed to improve understanding of the major evolutionary and ecological processes that shape the assemblage of amphibian and reptile communities to forest modifications. To this end, we compiled a global data set of amphibian and reptile surveys in natural, disturbed (burned, logged), and transformed (monocultures, polyspecific plantations) forest communities to assess the richness, phylogenetic diversity, and composition of those communities, as well as the morphological disparity among taxa between natural and modified forest habitats. Forest transformations led to a diversity reduction of 15.46% relative to the statistically nonsignificant effect of disturbances. Transformations also led to a community composition that was 39.4% dissimilar to that on natural forests, compared with 16.1% difference in disturbances. Modifications did not affect the morphological disparity of communities (p = 0.167 and 0.744), and we found little evidence of taxon-specific responses to anthropic impacts. Monocultures and polyspecific plantations detrimentally affected the conservation and ecological value of both amphibian and reptile communities and altered the evolutionary processes shaping these communities, whereas forests with lower impact disturbances might, to some extent, serve as reservoirs of species. Although different mechanisms might buffer the collapse of herpetological communities, preserving remaining natural forests is necessary for conserving communities in the face of future anthropic pressures.

Con el aumento del área cubierta por entornos modificados por el humano, cada vez es más importante entender las respuestas que tienen las comunidades a los nuevos hábitats creados, especialmente en los taxones sensibles y amenazados. El objetivo de este estudio es mejorar el conocimiento sobre los principales procesos evolutivos y ecológicos que condicionan el ensamblado de las comunidades de anfibios y reptiles ante las modificaciones forestales. Con este fin, compilamos un conjunto de datos globales de los censos de anfibios y reptiles en las comunidades forestales naturales, perturbadas (taladas, incendiadas) y transformadas (monocultivos, plantaciones poliespecíficas) para valorar la riqueza, diversidad filogenética y composición de aquellas comunidades, así como la disparidad morfológica entre los taxones entre los hábitats forestales naturales y modificados. Las transformaciones forestales llevaron a una reducción de 15.46% de la diversidad en relación al efecto sin significancia estadística de las perturbaciones. Las transformaciones también derivaron en una composición comunitaria que fue 39.4% diferente a la de los bosques naturales, en comparación con el 16.1% de diferencia en las perturbaciones. Las modificaciones no afectaron la disparidad morfológica de las comunidades (p = 0.167 y 0.744) y no encontramos suficiente evidencia de respuestas específicas por taxón a los impactos antrópicos. Los monocultivos y las plantaciones poliespecíficas afectaron negativamente a la conservación y al valor ecológico de las comunidades de anfibios y reptiles y alteraron los procesos evolutivos que condicionan a estas comunidades, mientras que los bosques menos impactados podrían, hasta cierto punto, actuar como reservorios de especies. Sin embargo, mientras que diferentes mecanismos pueden amortiguar el colapso de las comunidades herpetológicas, se requiere la conservación de los bosques naturales para preservar las comunidades que se enfrentarán a presiones antrópicas.

Signal detection shapes ornament allometry in functionally convergent Caribbean Anolis and Southeast Asian Draco lizards.

Visual ornaments have long been assumed to evolve hyper-allometry as an outcome of sexual selection. Yet growing evidence suggests many sexually selected morphologies can exhibit other scaling patterns with body size, including hypo-allometry. The large conspicuous throat fan, or dewlap, of arboreal Caribbean Anolis lizards was one ornament previously thought to conform to the classical expectation of hyper-allometry. We re-evaluated this classic example alongside a second arboreal group of lizards that has also independently evolved a functionally equivalent dewlap, the Southeast Asian Draco lizards. Across multiple closely related species in both genera, the Anolis and Draco dewlaps were either isometric or had hypo-allometric scaling patterns. In the case of the Anolis dewlap, variation in dewlap allometry was predicted by the distance of conspecifics and the light environment in which the dewlap was typically viewed. Signal efficacy, therefore, appears to have driven the evolution of hypo-allometry in what was originally thought to be a sexually selected ornament with hyper-allometry. Our findings suggest that other elaborate morphological structures used in social communication might similarly exhibit isometric or hypo-allometric scaling patterns because of environmental constraints on signal detection.

Costs of territoriality: a review of hypotheses, meta-analysis, and field study.

The evolution of territoriality reflects the balance between the benefit and cost of monopolising a resource. While the benefit of territoriality is generally intuitive (improved access to resources), our understanding of its cost is less clear. This paper combines: 1. a review of hypotheses and meta-analytic benchmarking of costs across diverse taxa; and 2. a new empirical test of hypotheses using a longitudinal study of free-living male territorial lizards. The cost of territoriality was best described as a culmination of multiple factors, but especially costs resulting from the time required to maintain a territory (identified by the meta-analysis) or those exacerbated by a territory that is large in size (identified by the empirical test). The meta-analysis showed that physiological costs such as energetic expenditure or stress were largely negligible in impact on territory holders. Species that used territories to monopolise access to mates appeared to incur the greatest costs, whereas those defending food resources experienced the least. The single largest gap in our current understanding revealed by the literature review is the potential cost associated with increased predation. There is also a clear need for multiple costs to be evaluated concurrently in a single species. The empirical component of this study showcases a powerful analytical framework for evaluating a range of hypotheses using correlational data obtained in the field. More broadly, this paper highlights key factors that should be considered in any investigation that attempts to account for the evolutionary origin or ecological variation in territorial behaviour within and between species.

Deep-time convergent evolution in animal communication presented by shared adaptations for coping with noise in lizards and other animals.

Convergence in communication appears rare compared with other forms of adaptation. This is puzzling, given communication is acutely dependent on the environment and expected to converge in form when animals communicate in similar habitats. We uncover deep-time convergence in territorial communication between two groups of tropical lizards separated by over 140 million years of evolution: the Southeast Asian Draco and Caribbean Anolis. These groups have repeatedly converged in multiple aspects of display along common environmental gradients. Robot playbacks to free-ranging lizards confirmed that the most prominent convergence in display is adaptive, as it improves signal detection. We then provide evidence from a sample of the literature to further show that convergent adaptation among highly divergent animal groups is almost certainly widespread in nature. Signal evolution is therefore curbed towards the same set of adaptive solutions, especially when animals are challenged with the problem of communicating effectively in noisy environments.

Conspicuous animal signals avoid the cost of predation by being intermittent or novel: confirmation in the wild using hundreds of robotic prey.

Social animals are expected to face a trade-off between producing a signal that is detectible by mates and rivals, but not obvious to predators. This trade-off is fundamental for understanding the design of many animal signals, and is often the lens through which the evolution of alternative communication strategies is viewed. We have a reasonable working knowledge of how conspecifics detect signals under different conditions, but how predators exploit conspicuous communication of prey is complex and hard to predict. We quantified predation on 1566 robotic lizard prey that performed a conspicuous visual display, possessed a conspicuous ornament or remained cryptic. Attacks by free-ranging predators were consistent across two contrasting ecosystems and showed robotic prey that performed a conspicuous display were equally likely to be attacked as those that remained cryptic. Furthermore, predators avoided attacking robotic prey with a fixed, highly visible ornament that was novel at both locations. These data show that it is prey familiarity-not conspicuousness-that determine predation risk. These findings replicated across different predator-prey communities not only reveal how conspicuous signals might evolve in high predation environments, but could help resolve the paradox of aposematism and why some exotic species avoid predation when invading new areas.

Gliding Dragons and Flying Squirrels: Diversifying versus Stabilizing Selection on Morphology following the Evolution of an Innovation.

Evolutionary innovations and ecological competition are factors often cited as drivers of adaptive diversification. Yet many innovations result in stabilizing rather than diversifying selection on morphology, and morphological disparity among coexisting species can reflect competitive exclusion (species sorting) rather than sympatric adaptive divergence (character displacement). We studied the innovation of gliding in dragons (Agamidae) and squirrels (Sciuridae) and its effect on subsequent body size diversification. We found that gliding either had no impact (squirrels) or resulted in strong stabilizing selection on body size (dragons). Despite this constraining effect in dragons, sympatric gliders exhibit greater size disparity compared with allopatric gliders, a pattern consistent with, although not exclusively explained by, ecological competition changing the adaptive landscape of body size evolution to induce character displacement. These results show that innovations do not necessarily instigate further differentiation among species, as is so often assumed, and suggest that competition can be a powerful force generating morphological divergence among coexisting species, even in the face of strong stabilizing selection.

Walk, swim or fly? Locomotor mode predicts genetic differentiation in vertebrates.

Limited dispersal is commonly used to explain differences in diversification rates. An obvious but unexplored factor affecting dispersal is the mode of locomotion used by animals. Whether individuals walk, swim or fly can dictate the type and severity of geographical barriers to dispersal, and determine the general range over which genetic differentiation might occur. We collated information on locomotion mode and genetic differentiation (FST ) among vertebrate populations from over 400 published articles. Our results showed that vertebrate species that walk tend to have higher genetic differentiation among populations than species that swim or fly. Within species that swim, vertebrates in freshwater systems have higher genetic differentiation than those in marine systems, which is consistent with the higher number of species in freshwater environments. These results show that locomotion mode can impact gene flow among populations, supporting at a broad-scale what has previously been proposed at smaller taxonomical scales.

Manipulation of habitat isolation and area implicates deterministic factors and limited neutrality in community assembly.

Theory predicts deterministic and stochastic factors will contribute to community assembly in different ways: Environmental filters should regulate those species that establish in a particular area resulting in the ecological requirements of species being the primary driver of species distributions, while chance and dispersal limitation should dictate the likelihood of species reaching certain areas with the ecology of species being largely neutral. These factors are specifically relevant for understanding how the area and isolation of different habitats or islands interact to affect community composition. Our review of the literature found few experimental studies have examined the interactive effect of habitat area and isolation on community assembly, and the results of those experiments have been mixed. We manipulated the area and isolation of rock "islands" created de novo in a grassland matrix to experimentally test how deterministic and stochastic factors shape colonizing animal communities. Over 64 weeks, the experiment revealed the primacy of deterministic factors in community assembly, with habitat islands of the same size exhibiting remarkable consistency in community composition and diversity, irrespective of isolation. Nevertheless, tangible differences still existed in abundance inequality among taxa: Large, near islands had consistently higher numbers of common taxa compared to all other island types. Dispersal limitation is often assumed to be negligible at small spatial scales, but our data shows this not to be the case. Furthermore, the dispersal limitation of a subset of species has potentially complex flow-on effects for dictating the type of deterministic factors affecting other colonizing species.

Ecological Release from Aquatic Predation Is Associated with the Emergence of Marine Blenny Fishes onto Land.

An ecological release from competition or predation is a frequent adaptive explanation for the colonization of novel environments, but empirical data are limited. On the island of Rarotonga, several blenny fish species appear to be in the process of colonizing land. Anecdotal observations have implied that aquatic predation is an important factor in prompting such amphibious fish behavior. We provide evidence supporting this hypothesis by demonstrating that amphibious blennies shift their abundance up and down the shoreline to remain above predatory fishes that periodically move into intertidal areas during high tide. A predation experiment using blenny mimics confirmed a high risk of aquatic predation for blennies, significantly higher than predation experienced on land. These data suggest that predation has played an active role in promoting terrestrial activity in amphibious blennies and provide a rare example of how ecological release from predation could drive the colonization of a novel environment.

Gliding lizards use the position of the sun to enhance social display.

Effective communication requires animal signals to be readily detected by receivers in the environments in which they are typically given. Certain light conditions enhance the visibility of colour signals and these conditions can vary depending on the orientation of the sun and the position of the signaller. We tested whether Draco sumatranus gliding lizards modified their position relative to the sun to enhance the conspicuousness of their throat-fan (dewlap) during social display to conspecifics. The dewlap was translucent, and we found that lizards were significantly more likely to orient themselves perpendicular to the sun when displaying. This increases the dewlap's radiance, and likely, its conspicuousness, by increasing the amount of light transmitted through the ornament. This is a rare example of a behavioural adaptation for enhancing the visibility of an ornament to distant receivers.

Many Paths to a Common Destination: Morphological Differentiation of a Functionally Convergent Visual Signal.

Understanding the interacting outcomes of selection and historical contingency in shaping adaptive evolution remains a challenge in evolutionary biology. While selection can produce convergent outcomes when species occupy similar environments, the unique history of each species can also influence evolutionary trajectories and result in different phenotypic end points. The question is to what extent historical contingency places species on different adaptive pathways and, in turn, the extent to which we can predict evolutionary outcomes. Among lizards there are several distantly related genera that have independently evolved an elaborate extendible dewlap for territorial communication. We conducted a detailed morphological study and employed new phylogenetic comparative methods to investigate the evolution of the underlying hyoid that powers the extension of the dewlap. This analysis showed that there appear to have been multiple phenotypic pathways for evolving a functionally convergent dewlap. The biomechanical complexity that underlies this morphological structure implies that adaptation should have been constrained to a narrow phenotypic pathway. However, multiple adaptive solutions have been possible in apparent response to a common selection pressure. Thus, the phenotypic outcome that subsequently evolved in different genera seems to have been contingent on the history of the group in question. This blurs the distinction between convergent and historically contingent adaptation and suggests that adaptive phenotypic diversity can evolve without the need for divergent natural selection.

Repeated evolution of amphibious behavior in fish and its implications for the colonization of novel environments.

We know little about on how frequently transitions into new habitats occur, especially the colonization of novel environments that are the most likely to instigate adaptive evolution. One of the most extreme ecological transitions has been the shift in habitat associated with the move from water to land by amphibious fish. We provide the first phylogenetic investigation of these transitions for living fish. Thirty-three families have species reported to be amphibious and these are likely independent evolutionary origins of fish emerging onto land. Phylogenetic reconstructions of closely related taxa within one of these families, the Blenniidae, inferred as many as seven convergences on a highly amphibious lifestyle. Taken together, there appear to be few constraints on fish emerging onto land given amphibious behavior has evolved repeatedly many times across ecologically diverse families. The colonization of novel habitats by other taxa resulting in less dramatic changes in environment should be equally, if not, more frequent in nature, providing an important prerequisite for subsequent adaptive differentiation.

Understanding the Spatial Scale of Genetic Connectivity at Sea: Unique Insights from a Land Fish and a Meta-Analysis.

Quantifying the spatial scale of population connectivity is important for understanding the evolutionary potential of ecologically divergent populations and for designing conservation strategies to preserve those populations. For marine organisms like fish, the spatial scale of connectivity is generally set by a pelagic larval phase. This has complicated past estimates of connectivity because detailed information on larval movements are difficult to obtain. Genetic approaches provide a tractable alternative and have the added benefit of estimating directly the reproductive isolation of populations. In this study, we leveraged empirical estimates of genetic differentiation among populations with simulations and a meta-analysis to provide a general estimate of the spatial scale of genetic connectivity in marine environments. We used neutral genetic markers to first quantify the genetic differentiation of ecologically-isolated adult populations of a land dwelling fish, the Pacific leaping blenny (Alticus arnoldorum), where marine larval dispersal is the only probable means of connectivity among populations. We then compared these estimates to simulations of a range of marine dispersal scenarios and to collated FST and distance data from the literature for marine fish across diverse spatial scales. We found genetic connectivity at sea was extensive among marine populations and in the case of A. arnoldorum, apparently little affected by the presence of ecological barriers. We estimated that ~5000 km (with broad confidence intervals ranging from 810-11,692 km) was the spatial scale at which evolutionarily meaningful barriers to gene flow start to occur at sea, although substantially shorter distances are also possible for some taxa. In general, however, such a large estimate of connectivity has important implications for the evolutionary and conservation potential of many marine fish communities.

Land colonisation by fish is associated with predictable changes in life history.

The colonisation of new environments is a central evolutionary process, yet why species make such transitions often remains unknown because of the difficulty in empirically investigating potential mechanisms. The most likely explanation for transitions to new environments is that doing so conveys survival benefits, either in the form of an ecological release or new ecological opportunity. Life history theory makes explicit predictions about how traits linked to survival and reproduction should change with shifts in age-specific mortality. We used these predictions to examine whether a current colonisation of land by fishes might convey survival benefits. We found that blenny species with more terrestrial lifestyles exhibited faster reproductive development and slower growth rates than species with more marine lifestyles; a life history trade off that is consistent with the hypothesis that mortality has become reduced in younger life stages on land. A plausible explanation for such a shift is that an ecological release or opportunity on land has conveyed survival benefits relative to the ancestral marine environment. More generally, our study illustrates how life history theory can be leveraged in novel ways to formulate testable predictions on why organisms might make transitions into novel environments.

Population Variation in the Life History of a Land Fish, Alticus arnoldorum, and the Effects of Predation and Density.

Life history variation can often reflect differences in age-specific mortality within populations, with the general expectation that reproduction should be shifted away from ages experiencing increased mortality. Investigators of life history in vertebrates frequently focus on the impact of predation, but there is increasing evidence that predation may have unexpected impacts on population density that in turn prompt unexpected changes in life history. There are also other reasons why density might impact life history independently of predation or mortality more generally. We investigated the consequences of predation and density on life history variation among populations of the Pacific leaping blenny, Alticus arnoldorum. This fish from the island of Guam spends its adult life out of the water on rocks in the splash zone, where it is vulnerable to predation and can be expected to be sensitive to changes in population density that impact resource availability. We found populations invested more in reproduction as predation decreased, while growth rate varied primarily in response to population density. These differences in life history among populations are likely plastic given the extensive gene flow among populations revealed by a previous study. The influence of predation and density on life history was unlikely to have operated independently of each other, with predation rate tending to be associated with reduced population densities. Taken together, our results suggest predation and density can have complex influences on life history, and that plastic life history traits could allow populations to persist in new or rapidly changing environments.

Repeated evolution and the impact of evolutionary history on adaptation.

BACKGROUND: Whether natural selection can erase the imprint of past evolutionary history from phenotypes has been a topic of much debate. A key source of evidence that present-day selection can override historically contingent effects comes from the repeated evolution of similar adaptations in different taxa. Yet classic examples of repeated evolution are often among closely related taxa, suggesting the likelihood that similar adaptations evolve is contingent on the length of time separating taxa. To resolve this, we performed a meta-analysis of published reports of repeated evolution. RESULTS: Overall, repeated evolution was far more likely to be documented among closely related than distantly related taxa. However, not all forms of adaptation seemed to exhibit the same pattern. The evolution of similar behavior and physiology seemed frequent in distantly related and closely related taxa, while the repeated evolution of morphology was heavily skewed towards closely related taxa. Functionally redundant characteristics-alternative phenotypes that achieve the same functional outcome-also appeared less contingent. CONCLUSIONS: If the literature provides a reasonable reflection of the incidence of repeated evolution in nature, our findings suggest that natural selection can overcome contingent effects to an extent, but it depends heavily on the aspect of the phenotype targeted by selection.

How populations differentiate despite gene flow: sexual and natural selection drive phenotypic divergence within a land fish, the Pacific leaping blenny.

BACKGROUND: Divergence between populations in reproductively important features is often vital for speciation. Many studies attempt to identify the cause of population differentiation in phenotype through the study of a specific selection pressure. Holistic studies that consider the interaction of several contrasting forms of selection are more rare. Most studies also fail to consider the history of connectivity among populations and the potential for genetic drift or gene flow to facilitate or limit phenotypic divergence. We examined the interacting effects of natural selection, sexual selection and the history of connectivity on phenotypic differentiation among five populations of the Pacific leaping blenny (Alticus arnoldorum), a land fish endemic to the island of Guam. RESULTS: We found key differences among populations in two male ornaments--the size of a prominent head crest and conspicuousness of a coloured dorsal fin--that reflected a trade-off between the intensity of sexual selection (male biased sex ratios) and natural selection (exposure to predators). This differentiation in ornamentation has occurred despite evidence suggesting extensive gene flow among populations, which implies that the change in ornament expression has been recent (and potentially plastic). CONCLUSIONS: Our study provides an early snapshot of divergence in reproductively important features that, regardless of whether it reflects genetic or plastic changes in phenotype, could ultimately form a reproductive barrier among populations.

Habitat partitioning and morphological differentiation: the Southeast Asian Draco lizards and Caribbean Anolis lizards compared.

Sympatric species that initially overlap in resource use are expected to partition the environment in ways that will minimize interspecific competition. This shift in resource use can in turn prompt evolutionary changes in morphology. A classic example of habitat partitioning and morphological differentiation are the Caribbean Anolis lizards. Less well studied, but nevertheless striking analogues to the Anolis are the Southeast Asian Draco lizards. Draco and Anolis have evolved independently of each other for at least 80 million years. Their comparison subsequently offers a special opportunity to examine mechanisms of phenotypic differentiation between two ecologically diverse, but phylogenetically distinct groups. We tested whether Draco shared ecological axes of differentiation with Anolis (e.g., habitat use), whether this differentiation reflected interspecific competition, and to what extent adaptive change in morphology has occurred along these ecological axes. Using existing data on Anolis, we compared the habitat use and morphology of Draco in a field study of allopatric and sympatric species on the Malay Peninsula, Borneo and in the Philippines. Sympatric Draco lizards partitioned the environment along common resource axes to the Anolis lizards, especially in perch use. Furthermore, the morphology of Draco was correlated with perch use in the same way as it was in Anolis: species that used wider perches exhibited longer limb lengths. These results provide an important illustration of how interspecific competition can occur along common ecological axes in different animal groups, and how natural selection along these axes can generate the same type of adaptive change in morphology.

The social network and communicative complexity: preface to theme issue.

The complex social worlds of many animal species may be linked to complex communicative systems in those species. We now have evidence in diverse taxa and in different communicative modalities suggesting that complexity in social groups can drive complexity in signalling systems. The aim of this theme issue is to develop the theory behind this link between social complexity and communicative complexity, and to provide an overview of the lines of research testing this link.