Daniel Pincheira-Donoso

The evolution of body size under environmental gradients in ectotherms: why should Bergmann's rule apply to lizards?

BackgroundThe impact of environmental gradients on the evolution of life history traits is a central issue in macroecology and evolutionary biology. A number of hypotheses have been formulated to explain factors shaping patterns of variation in animal mass. One such example is Bergmanns rule, which predicts that body size will be positively correlated with latitude and elevation, and hence, with decreasing environmental temperatures. A generally accepted explanation for this phenotypic response is that as body mass increases, body surface area gets proportionally smaller, which contributes to reduced rates of heat-loss. Phylogenetic and non-phylogenetic evidence reveals that endotherms follow Bergmanns rule. In contrast, while previous non-phylogenetic studies supported this prediction in up to 75% of ectotherms, recent phylogenetic comparative analyses suggest that its validity for these organisms is controversial and less understood. Moreover, little attention has been paid to why some ectotherms conform to this rule, while others do not. Here, we investigate Bergmanns rule in the six main clades forming the Liolaemus genus, one of the largest and most environmentally diverse genera of terrestrial vertebrates. A recent study conducted on some species belonging to four of these six clades concluded that Liolaemus species follow Bergmanns rule, representing the only known phylogenetic support for this model in lizards. However, a later reassessment of this evidence, performed on one of the four analysed clades, produced contrasting conclusions.ResultsOur results fail to support Bergmanns rule in Liolaemus lizards. Non-phylogenetic and phylogenetic analyses showed that none of the studied clades experience increasing body size with increasing latitude and elevation.ConclusionMost physiological and behavioural processes in ectotherms depend directly upon their body temperature. In cold environments, adaptations to gain heat rapidly are under strong positive selection to allow optimal feeding, mating and predator avoidance. Therefore, evolution of larger body size in colder environments appears to be a disadvantageous thermoregulatory strategy. The repeated lack of support for Bergmanns rule in ectotherms suggests that this model should be recognized as a valid rule exclusively for endotherms.

Global Taxonomic Diversity of Living Reptiles

Reptiles are one of the most ecologically and evolutionarily remarkable groups of living organisms, having successfully colonized most of the planet, including the oceans and some of the harshest and more environmentally unstable ecosystems on earth. Here, based on a complete dataset of all the world’s diversity of living reptiles, we analyse lineage taxonomic richness both within and among clades, at different levels of the phylogenetic hierarchy. We also analyse the historical tendencies in the descriptions of new reptile species from Linnaeus to March 2012. Although (non-avian) reptiles are the second most species-rich group of amniotes after birds, most of their diversity (96.3%) is concentrated in squamates (59% lizards, 35% snakes, and 2% amphisbaenians). In strong contrast, turtles (3.4%), crocodilians (0.3%), and tuataras (0.01%) are far less diverse. In terms of species discoveries, most turtles and crocodilians were described early, while descriptions of lizards, snakes and amphisbaenians are multimodal with respect to time. Lizard descriptions, in particular, have reached unprecedented levels during the last decade. Finally, despite such remarkably asymmetric distributions of reptile taxonomic diversity among groups, we found that the distributions of lineage richness are consistently right-skewed, with most clades (monophyletic families and genera) containing few lineages (monophyletic genera and species, respectively), while only a few have radiated greatly (notably the families Colubridae and Scincidae, and the lizard genera Anolis and Liolaemus). Therefore, such consistency in the frequency distribution of richness among clades and among phylogenetic levels suggests that the nature of reptile biodiversity is fundamentally fractal (i.e., it is scale invariant). We then compared current reptile diversity with the global reptile diversity and taxonomy known in 1980. Despite substantial differences in the taxonomies (relative to 2012), the patterns of lineage richness remain qualitatively identical, hence reinforcing our conclusions about the fractal nature of reptile biodiversity.

Fecundity Selection and the Evolution of Reproductive Output and Sex-Specific Body Size in the Liolaemus Lizard Adaptive Radiation

Fecundity is a primary component of fitness. Theory predicts that the evolution of fecundity through increased brood size results from fecundity selection favouring larger female size to accommodate more offspring and to store more energy. This is expected to generate asymmetric selection on body size between the sexes, ultimately driving evolution of female-biased sexual size dimorphism. Additionally, it has been predicted that the intensity of fecundity selection increases when the opportunities for reproduction are reduced by the limiting thermal effects of increasing latitude-elevation (i.e. decreasing environmental temperatures) on the length of the reproductive season. This later factor would be particularly strong among ectotherms, where reproduction is heavily temperature-dependent. However, this integrative perspective on reproductive evolution by fecundity selection has rarely been investigated. Here, we employ a comparative approach to investigate these predictions in Liolaemus, a prominent lizard radiation. As expected, Liolaemus reproductive output (i.e. offspring number per reproductive episode) increases predictably with increasing female size. However, contrary to predictions, we found that increased fecundity does not translate into female-biased SSD, and that combined latitude-elevation does not impose a detectable effect on fecundity. Finally, our allometric analyses reveal that SSD scales with body size, which supports the occurrence of Rensch’s rule in these lizards. We discuss the evolutionary implications of our results, and the assumptions of the investigated hypotheses.

A phylogenetic analysis of sex-specific evolution of ecological morphology in Liolaemus lizards

Adaptive radiation theory predicts that phenotypic traits involved in ecological performance evolve in different directions in populations subjected to divergent natural selection, resulting in the evolution of ecological diversity. This idea has largely been supported through comparative studies exploring relationships between ecological preferences and quantitative traits among different species. However, intersexual perspectives are often ignored. Indeed, although it is well established that intersexual competition and sex-specific parental and reproductive roles may often subject sex-linked phenotypes to antagonistic selection effects, most ecomorphological research has explored adaptive evolution on a single sex, or on means obtained from both sexes together. The few studies taking sexual differences into account reveal the occurrence of sex-specific ecomorphs in some clades of lizards, and conclude that the independent contribution of the sexes to the morphological diversity produced by adaptive radiation can be substantial. Here, we investigate whether microhabitat use results in the evolution of sex-specific ecomorphs across 44 Liolaemus lizard species. We found that microhabitat structure does not predict variation in body size and shape in either of the sexes. Yet, we found that males and females tend to occupy significantly different positions in multivariate morphological spaces, indicating that treating males and females as ecologically and phenotypically equivalent units may lead to incomplete or mistaken estimations of the diversity produced by adaptive evolution.

Body size evolution in South American Liolaemus lizards of the boulengeri clade: a contrasting reassessment

Bergmanns rule predicts larger body sizes in species living in higher latitudes and altitudes. This rule appears to be valid for endotherms, but its relevance to ectotherm vertebrates has largely been debated. In squamate reptiles (lizards and snakes), only one study, based on Liolaemus species of the boulengeri clade, has provided phylogenetic evidence in favour of Bergmanns clines. We reassessed this model in the same lizard clade, using a more representative measure of species body size and including a larger number of taxa in the sample. We found no evidence to support Bergmanns rule in this lineage. However, these non‐significant results appear to be explained only by the inclusion of further species rather than by a different estimation of body size. Analyses conducted on the 16 species included in the previous study always revealed significant relationships between body size and latitude–altitude, whereas, the enlarged sample always rejected the pattern predicted by Bergmanns rule.

The balance between predictions and evidence and the search for universal macroecological patterns: taking Bergmann's rule back to its endothermic origin

Geographical variation in environmental temperatures is expected to impose clinal phenotypic selection that results in the expression of large-scale gradients of body mass variation within animal clades. Body size is predicted to increase with increasing latitude and elevation, and hence, with decreasing temperature, a pattern broadly known as Bergmann’s rule. However, empirical observations are highly conflicting. Whilst most studies support this prediction in endotherms (birds and mammals), analyses conducted on ectotherms often fail to report this pattern. Does it reduce the validity of this macroecological rule? Since the original formulation of Bergmann’s rule only involved endothermic organisms, I argue that the controversy is not a consequence of its predictive power, but a result of the later inclusion of ectotherms as part of the prediction. Here, I propose that the common conception of Bergmann’s rule maintained for half a century is changed back to its original definition restricted to endotherms. This temperature–size relationship might therefore consolidate as a well-established macroecological rule if its original formulation is respected. Finally, I develop these claims on my initial suggestion that Bergmann’s rule should be recognized as the evolutionary outcome of a general process with no phylogenetic scale distinction of species or populations, being equally applicable amongst and within species.

What defines an adaptive radiation? Macroevolutionary diversification dynamics of an exceptionally species-rich continental lizard radiation.

BackgroundAdaptive radiation theory posits that ecological opportunity promotes rapid proliferation of phylogenetic and ecological diversity. Given that adaptive radiation proceeds via occupation of available niche space in newly accessed ecological zones, theory predicts that: (i) evolutionary diversification follows an ‘early-burst’ process, i.e., it accelerates early in the history of a clade (when available niche space facilitates speciation), and subsequently slows down as niche space becomes saturated by new species; and (ii) phylogenetic branching is accompanied by diversification of ecologically relevant phenotypic traits among newly evolving species. Here, we employ macroevolutionary phylogenetic model-selection analyses to address these two predictions about evolutionary diversification using one of the most exceptionally species-rich and ecologically diverse lineages of living vertebrates, the South American lizard genus Liolaemus.ResultsOur phylogenetic analyses lend support to a density-dependent lineage diversification model. However, the lineage through-time diversification curve does not provide strong support for an early burst. In contrast, the evolution of phenotypic (body size) relative disparity is high, significantly different from a Brownian model during approximately the last 5 million years of Liolaemus evolution. Model-fitting analyses also reject the ‘early-burst’ model of phenotypic evolution, and instead favour stabilizing selection (Ornstein-Uhlenbeck, with three peaks identified) as the best model for body size diversification. Finally, diversification rates tend to increase with smaller body size.ConclusionsLiolaemus have diversified under a density-dependent process with slightly pronounced apparent episodic pulses of lineage accumulation, which are compatible with the expected episodic ecological opportunity created by gradual uplifts of the Andes over the last ~25My. We argue that ecological opportunity can be strong and a crucial driver of adaptive radiations in continents, but may emerge less frequently (compared to islands) when major events (e.g., climatic, geographic) significantly modify environments. In contrast, body size diversification conforms to an Ornstein-Uhlenbeck model with multiple trait optima. Despite this asymmetric diversification between both lineages and phenotype, links are expected to exist between the two processes, as shown by our trait-dependent analyses of diversification. We finally suggest that the definition of adaptive radiation should not be conditioned by the existence of early-bursts of diversification, and should instead be generalized to lineages in which species and ecological diversity have evolved from a single ancestor.

Fecundity selection theory: concepts and evidence

Fitness results from an optimal balance between survival, mating success and fecundity. The interactions between these three components of fitness vary depending on the selective context, from positive covariation between them, to antagonistic pleiotropic relationships when fitness increases in one reduce the fitness of others. Therefore, elucidating the routes through which selection shapes life history and phenotypic adaptations via these fitness components is of primary significance to understanding ecological and evolutionary dynamics. However, while the fitness components mediated by natural (survival) and sexual (mating success) selection have been debated extensively from most possible perspectives, fecundity selection remains considerably less studied. Here, we review the theoretical basis, evidence and implications of fecundity selection as a driver of sex‐specific adaptive evolution. Based on accumulating literature on the life‐history, phenotypic and ecological aspects of fecundity, we (i) suggest a re‐arrangement of the concepts of fecundity, whereby we coin the term ‘transient fecundity’ to refer to brood size per reproductive episode, while ‘annual’ and ‘lifetime fecundity’ should not be used interchangeably with ‘transient fecundity’ as they represent different life‐history parameters; (ii) provide a generalized re‐definition of the concept of fecundity selection as a mechanism that encompasses any traits that influence fecundity in any direction (from high to low) and in either sex; (iii) review the (macro)ecological basis of fecundity selection (e.g. ecological pressures that influence predictable spatial variation in fecundity); (iv) suggest that most ecological theories of fecundity selection should be tested in organisms other than birds; (v) argue that the longstanding fecundity selection hypothesis of female‐biased sexual size dimorphism (SSD) has gained inconsistent support, that strong fecundity selection does not necessarily drive female‐biased SSD, and that this form of SSD can be driven by other selective pressures; and (vi) discuss cases in which fecundity selection operates on males. This conceptual analysis of the theory of fecundity selection promises to help illuminate one of the central components of fitness and its contribution to adaptive evolution.

Testing the Accuracy of Fecal-Based Analyses in Studies of Trophic Ecology in Lizards

Abstract Trophic niche studies are essential for evaluating ecological interactions between and within species and their evolutionary implications. For example, fundamental aspects of a wide range of hypotheses concerning population divergence, evolution of sexual dimorphism, and adaptations to fluctuating environments rely on dietary evidence. The accuracy of different methodologies used to estimate trophic specializations is therefore a fundamental issue. Under the assumption that direct observations of gastric contents provide accurate information about dietary preferences, I examined how reliably diet is reflected in fecal pellets. I conducted two main comparative tests on living lizards. First, I fed individuals of 23 species with hard- and soft-bodied organisms, and compared fecal pellets. Second, I examined prey items from natural diets represented in feces and gastric contents (stomach-flushing) in a wild population of the lizard Liolaemus tenuis. My results reveal that fecal samples provide inaccurate estimates of lizard trophic preferences, mainly because soft-bodied organisms are destroyed by digestive processes. Even though soft-bodied prey may be essential dietary items (as inferred from gastric analysis), these organisms may be almost entirely absent from feces. I suggest that direct gastric analyses should be the preferred method for analyzing reptilian diets.

The genetic architecture of sexual conflict: male harm and female resistance in Callosobruchus maculatus

Males harm females during mating in a range of species. This harm is thought to evolve because it is directly or indirectly beneficial to the male, despite being costly to his mate. The resulting sexually antagonistic selection can cause sexual arms races. For sexually antagonistic co‐evolution to occur, there must be genetic variation for traits involved in female harming and susceptibility to harm, but even then intersexual genetic correlations could facilitate or impede sexual co‐evolution. Male Callosobruchus maculatus harm their mates during copulation by damaging the female’s reproductive tract. However, there have been no investigations of the genetic variation in damage or in female susceptibility to damage, nor has the genetic covariance between these characters been assessed. Here, we use a full‐sib/half‐sib breeding design to show that male damage is heritable, whereas female susceptibility to damage is much less so. There is also a substantial positive genetic correlation between the two, suggesting that selection favouring damaging males will increase the prevalence of susceptible females. We also provide evidence consistent with intralocus sexual conflict in this species.