The macroecology of chemical communication in lizards: do climatic factors drive the evolution of signalling glands?

Chemical communication plays a pivotal role in shaping sexual and ecological interactions among animals. In lizards, fundamental mechanisms of sexual selection such as female mate choice have rarely been shown to be influenced by quantitative phenotypic traits (e.g., ornaments), while chemical signals have been found to potentially influence multiple forms of sexual and social interactions, including mate choice and territoriality. Chemical signals in lizards are secreted by glands primarily located on the edge of the cloacae (precloacal glands, PG) and thighs (femoral glands), and whose interspecific and interclade number ranges from 0 to >100. However, elucidating the factors underlying the evolution of such remarkable variation remains an elusive endeavour. Competing hypotheses suggest a dominant role for phylogenetic conservatism (i.e., species within clades share similar numbers of glands) or for natural selection (i.e., their adaptive diversification results in deviating numbers of glands from ancestors). Using the prolific Liolaemus lizard radiation from South America (where precloacal glands vary from 0-14), we present one of the largest-scale tests of both hypotheses to date. Based on climatic and phylogenetic modelling, we show a clear role for both phylogenetic inertia and adaptation underlying gland variation: (i) solar radiation, net primary productivity, topographic heterogeneity and precipitation range have a significant effect on number of PG variation, (ii) humid and cold environments tend to concentrate species with a higher number of glands, (iii) there is a strong phylogenetic signal that tends to conserve the number of PG within clades. Collectively, our study confirms that the inertia of niche conservatism can be broken down by the need of species facing different selection regimes to adjust their glands to suit the demands of their specific environments

Defences against brood parasites from a social immunity perspective

Parasitic interactions are so ubiquitous that all multicellular organisms have evolved a system of defences to reduce their costs, whether the parasites they encounter are the “classic parasites” that feed on the individual, or “brood parasites” that usurp parental care. Many parallels have been drawn between defences deployed against both types of parasite, but typically, whilst defences against classic parasites have been selected to protect survival, those against brood parasites have been selected to protect the parent’s inclusive fitness, suggesting that the selection pressures they impose are fundamentally different. However, there is another class of defences against classic parasites that have specifically been selected to protect an individual’s inclusive fitness, known as “social immunity”. Social immune responses include the anti-parasite defences typically provided for others in kin-structured groups, such as the antifungal secretions produced by termite workers to protect the brood. Defences against brood parasites, therefore, are more closely aligned with social immune responses. Much like social immunity, host defences against brood parasitism are employed by a donor (a parent) for the benefit of one or more recipients (typically kin), and as with social defences against classic parasites, defences have therefore evolved to protect the donor’s inclusive fitness, not the survival or ultimately the fitness of individual recipients This can lead to severe conflicts between the different parties, whose interests are not always aligned. Here we consider defences against brood parasitism in the light of social immunity, at different stages of parasite encounter, addressing where conflicts occur and how they might be resolved. We finish with considering how this approach could help us to address longstanding questions in our understanding of brood parasitism.Peer reviewe

Global terrestrial distribution of penguins (Spheniscidae) and their conservation by protected areas

Establishing protected areas (PAs) ranks among the top priority actions to mitigate the global scale of modern biodiversity declines. However, the distribution of biodiversity is spatially asymmetric among regions and lineages, and the extent to which PAs offer effective protection for species and ecosystems remains uncertain. Penguins, regarded as prime bioindicator birds of the ecological health of their terrestrial and marine habitats, represent priority targets for such quantitative assessments. Of the world’s 18 penguin species, eleven are undergoing population declines, for which ten are classified as ‘Vulnerable’ or ‘Endangered’. Here, we employ a global-scale dataset to quantify the extent to which their terrestrial breeding areas are currently protected by PAs. Using quantitative methods for spatial ecology, we compare the global distribution of penguin colonies, including range and population size analyses, with the distribution of terrestrial PAs classified by the International Union for Conservation of Nature, and generate hotspot and endemism maps worldwide. Our assessment quantitatively reveals < 40% of the terrestrial range of eleven penguin species is currently protected, and that range size is the significant factor in determining PA protection. We also show that there are seven global hotspots of penguin biodiversity where four or five penguin species breed. We suggest that future penguin conservation initiatives should be implemented based on more comprehensive, quantitative assessments of the multi-dimensional interactions between areas and species to further the effectiveness of PA networks

Live fast, diversify non-adaptively: evolutionary diversification of exceptionally short-lived annual killifishes

Background: Adaptive radiations are triggered by ecological opportunity – the access to novel niche domains with abundant available resources that facilitate the formation of new ecologically divergent species. Therefore, as new species saturate niche space, clades experience a diversity-dependent slowdown of diversification over time. At the other extreme of the radiation continuum, non-adaptively radiating lineages undergo diversification with minimal niche differentiation when ‘spatial opportunity’ (i.e. areas with suitable ‘ancestral’ ecological conditions) is available. Traditionally, most research has focused on adaptive radiations, while empirical studies on non-adaptive radiations remain lagging behind. A prolific clade of African fish with extremely short lifespan (Nothobranchius killifish), show the key evolutionary features of a candidate non-adaptive radiation – primarily allopatric species with minimal niche and phenotypic divergence. Here, we test the hypothesis that Nothobranchius killifish have non-adaptively diversified. We employ phylogenetic modelling to investigate the tempo and mode of macroevolutionary diversification of these organisms. Results: Nothobranchius diversification has proceeded with minor niche differentiation and minimal morphological disparity among allopatric species. Additionally, we failed to identify evidence for a role of body size or biogeography in influencing diversification rates. Diversification has been homogeneous within this genus, with the only hotspot of species-richness not resulting from rapid diversification. However, species in sympatry show higher disparity, which may have been caused by character displacement among coexisting species. Conclusions: Nothobranchius killifish have proliferated following the tempo and mode of a non-adaptive radiation. Our study confirms that this exceptionally short-lived group have diversified with minimal divergent niche adaptation, while one group of coexisting species seems to have facilitated spatial overlap among these taxa via the evolution of ecological character displacement

Alternative reproductive adaptation predicts asymmetric responses to climate change in lizards

Anthropogenic climate change ranks among the major global-scale threats to modern biodiversity. Extinction risks are known to increase via the interactions between rapid climatic alterations and environmentally-sensitive species traits that fail to adapt to those changes. Accumulating evidence reveals the influence of ecophysiological, ecological and phenological factors as drivers underlying demographic collapses that lead to population extinctions. However, the extent to which life-history traits influence population responses to climate change remains largely unexplored. The emerging ‘cul-de-sac hypothesis’ predicts that reptilian viviparity (‘live-bearing’ reproduction), a ‘key innovation’ facilitating historical invasions of cold climates, increases extinction risks under progressively warming climates compared to oviparous reproduction – as warming advances polewards/mountainwards, historically cold-climates shrink, leading viviparous species to face demographic collapses. We present the first large-scale test of this prediction based on multiple lizard radiations and on future projections of climate-based ecological niche models. Viviparous species were found to experience stronger elevational range shifts (and potentially increased extinctions) in coming decades, compared to oviparous lizards. Therefore, our analyses support the hypothesis’s fundamental prediction that elevational shifts are more severe in viviparous species, and highlight the role that life-history adaptations play in the responses of biodiversity to ongoing climate change

Macroevolutionary diversification of glands for chemical communication in squamate reptiles

Chemical communication plays a central role in social, sexual and ecological interactions among animals. However, the macroevolutionary diversification of traits responsible for chemical signaling remains fundamentally unknown. Most research investigating evolutionary diversification of glands responsible for the production of chemical signals has focused on arthropods, while its study among vertebrates remains neglected. Using a global-scale dataset covering > 80% (7,904 species) of the living diversity of lizards and snakes (squamates), we investigate rates, trajectories and phylogenetic patterns of diversification of their follicular glands for chemical communication. We observed these glands in 13.66% of species, that their expression has varying phylogenetic signal among lineages, and that the crown squamate ancestor lacked follicular glands, which therefore originated and diversified subsequently during their evolutionary history. Additionally, our findings challenge the longstanding view that within squamates the Iguania are visually oriented while Scleroglossa are chemically-oriented, given that Iguania doubles Scleroglossa in the frequency of glands. Our phylogenetic analyses identified stabilizing selection as the best model describing follicular gland diversification, and revealed high rates of disparity. We provide the first global-scale analysis investigating the diversification of one of the main forms of communication among reptiles, presenting a macroevolutionary angle to questions traditionally explored at microevolutionary scale

Global patterns of body size evolution in squamate reptiles are not driven by climate

Aim: Variation in body size across animal species underlies most ecological and evolutionary processes shaping local- and large-scale patterns of biodiversity. For well over a century, climatic factors have been regarded as primary sources of natural selection on animal body size, and hypotheses such as Bergmann's rule (the increase of body size with decreasing temperature) have dominated discussions. However, evidence for consistent climatic effects, especially among ectotherms, remains equivocal. Here, we test a range of key hypotheses on climate-driven size evolution in squamate reptiles across several spatial and phylogenetic scales. Location: Global. Time period: Extant. Major taxa studied: Squamates (lizards and snakes). Methods: We quantified the role of temperature, precipitation, seasonality and net primary productivity as drivers of body mass across ca. 95% of extant squamate species (9,733 spp.). We ran spatial autoregressive models of phylogenetically corrected median mass per equal-area grid cell. We ran models globally, across separate continents and for major squamate clades independently. We also performed species-level analyses using phylogenetic generalized least square models and linear regressions of independent contrasts of sister species. Results: Our analyses failed to identify consistent spatial patterns in body size as a function of our climatic predictors. Nearly all continent- and family-level models differed from one another, and species-level models had low explanatory power. Main conclusions: The global distribution of body mass among living squamates varies independently from the variation in multiple components of climate. Our study, the largest in spatial and taxonomic scale conducted to date, reveals that there is little support for a universal, consistent mechanism of climate-driven size evolution within squamates

The global biogeography of lizard functional groups

Aim: Understanding the mechanisms determining species richness is a primary goal of biogeography. Richness patterns of sub-groups within a taxon are usually assumed to be driven by similar processes. However, if richness of distinct ecological strategies respond differently to the same processes, inferences made for an entire taxon may be misleading. We deconstruct the global lizard assemblage into functional groups and examine the congruence among richness patterns between them. We further examine the species richness – functional richness relationship to elucidate the way functional diversity contributes to the overall species richness patterns. Location: Global. Methods: Using comprehensive biological trait databases we classified the global lizard assemblage into ecological strategies based on body size, diet, activity times and microhabitat preferences, using Archetypal Analysis. We then examined spatial gradients in the richness of each strategy at the one-degree grid cell, biomes and realm scales. Results: We found that lizards can best be characterized by seven 'ecological strategies': scansorial, terrestrial, nocturnal, herbivorous, fossorial, large and semiaquatic. There are large differences among the global richness patterns of these strategies. While the major richness hotspot for lizards in general is in Australia, several strategies exhibit highest richness in the Amazon Basin. Importantly, the global maximum in lizard species richness is achieved at intermediate values of functional diversity and increasing functional diversity further result in a shallow decline of species richness. Main conclusions: The deconstruction of the global lizard assemblage along multiple ecological axes offers a new way to conceive lizard diversity patterns. It suggests that local lizard richness mostly increases when species belonging to particular ecological strategies become hyper-diverse there, and not because more ecological types are present in the most species rich localities. Thus maximum richness and maximum ecological diversity do not overlap. These results shed light on the global richness pattern of lizards, and highlight previously unidentified spatial patterns in understudied functional groups

Coalescent-based species delimitation in the sand lizards of the Liolaemus wiegmannii complex (Squamata: Liolaemidae)

Coalescent-based algorithms coupled with the access to genome-wide data have become powerful tools forassessing questions on recent or rapid diversification, as well as delineating species boundaries in the absence of reciprocal monophyly. In southern South America, the diversification of Liolaemus lizards during the Pleistocene is well documented and has been attributed to the climatic changes that characterized this recent period of time. Past climatic changes had harsh effects at extreme latitudes, including Patagonia, but habitat changes at intermediate latitudes of South America have also been recorded, including expansion of sand fields over northern Patagonia and Pampas). In this work, we apply a coalescent-based approach to study the diversification of the Liolaemus wiegmannii species complex, a morphologically conservative clade that inhabits sandy soils across northwest and south-central Argentina, and the south shores of Uruguay. Using four standard sequence markers (mitochondrial DNA and three nuclear loci) along with ddRADseq data we inferred species limits and a time calibrated species tree for the L. wiegmannii complex in order to evaluate the influence of Quaternary sand expansion/retraction cycles on diversification. We also evaluated the evolutionary independence of the recently described L. gardeli and inferred its phylogenetic position relative to L. wiegmannii. We find strong evidence for six allopatric candidate species within L. wiegmannii, which diversified during the Pleistocene. The Great Patagonian Glaciation (∼1 million years before present) likely split the species complex into two main groups: one composed of lineages associated with sub-Andean sedimentary formations, and the other mostly related to sand fields in the Pampas and northern Patagonia. We hypothesize that early speciation within L. wiegmannii was influenced by the expansion of sand dunes throughout central Argentina and Pampas. Finally, L. gardeli is supported as a distinct lineage nested within the L. wiegmannii complex.Fil: Villamil, Joaquín. Universidad de la República. Facultad de Ciencias; UruguayFil: Avila, Luciano Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico. Instituto Patagónico para el Estudio de los Ecosistemas Continentales; ArgentinaFil: Morando, Mariana. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico. Instituto Patagónico para el Estudio de los Ecosistemas Continentales; ArgentinaFil: Sites, Jack W.. University Brigham Young; Estados UnidosFil: Leaché, Adam D.. University of Washington; Estados UnidosFil: Maneyro, Raúl. Universidad de la República. Facultad de Ciencias; UruguayFil: Camargo Bentaberry, Arley. Universidad de la República; Urugua