Showing papers by "Jonathan B. Losos published in 2020"

Hurricane effects on Neotropical lizards span geographic and phylogenetic scales

Abstract: Extreme climate events such as droughts, cold snaps, and hurricanes can be powerful agents of natural selection, producing acute selective pressures very different from the everyday pressures acting on organisms. However, it remains unknown whether these infrequent but severe disruptions are quickly erased by quotidian selective forces, or whether they have the potential to durably shape biodiversity patterns across regions and clades. Here, we show that hurricanes have enduring evolutionary impacts on the morphology of anoles, a diverse Neotropical lizard clade. We first demonstrate a transgenerational effect of extreme selection on toepad area for two populations struck by hurricanes in 2017. Given this short-term effect of hurricanes, we then asked whether populations and species that more frequently experienced hurricanes have larger toepads. Using 70 y of historical hurricane data, we demonstrate that, indeed, toepad area positively correlates with hurricane activity for both 12 island populations of Anolis sagrei and 188 Anolis species throughout the Neotropics. Extreme climate events are intensifying due to climate change and may represent overlooked drivers of biogeographic and large-scale biodiversity patterns.

Phylogeographic and phenotypic outcomes of brown anole colonization across the Caribbean provide insight into the beginning stages of an adaptive radiation

Abstract: Some of the most important insights into the ecological and evolutionary processes of diversification and speciation have come from studies of island adaptive radiations, yet relatively little research has examined how these radiations initiate. We suggest that Anolis sagrei is a candidate for understanding the origins of the Caribbean Anolis adaptive radiation and how a colonizing anole species begins to undergo allopatric diversification, phenotypic divergence and, potentially, speciation. We undertook a genomic and morphological analysis of representative populations across the entire native range of A. sagrei, finding that the species originated in the early Pliocene, with the deepest divergence occurring between western and eastern Cuba. Lineages from these two regions subsequently colonized the northern Caribbean. We find that at the broadest scale, populations colonizing areas with fewer closely related competitors tend to evolve larger body size and more lamellae on their toepads. This trend follows expectations for post-colonization divergence from progenitors and convergence in allopatry, whereby populations freed from competition with close relatives evolve towards common morphological and ecological optima. Taken together, our results show a complex history of ancient and recent Cuban diaspora with populations on competitor-poor islands evolving away from their ancestral Cuban populations regardless of their phylogenetic relationships, thus providing insight into the original diversification of colonist anoles at the beginning of the radiation. Our research also supplies an evolutionary framework for the many studies of this increasingly important species in ecological and evolutionary research.

Bridging the Process-Pattern Divide to Understand the Origins and Early Stages of Adaptive Radiation: A Review of Approaches With Insights From Studies of Anolis Lizards

Abstract: Understanding the origins and early stages of diversification is one of the most elusive tasks in adaptive radiation research. Classical approaches, which aim to infer past processes from present-day patterns of biological diversity, are fraught with difficulties and assumptions. An alternative approach has been to study young clades of relatively few species, which may represent the putative early stages of adaptive radiation. However, it is difficult to predict whether those groups will ever reach the ecological and morphological disparity observed in the sorts of clades usually referred to as adaptive radiations, thereby making their utility in informing the early stages of such radiations uncertain. Caribbean Anolis lizards are a textbook example of an adaptive radiation; anoles have diversified independently on each of the 4 islands in the Greater Antilles, producing replicated radiations of phenotypically diverse species. However, the underlying processes that drove these radiations occurred 30-65 million years ago and so are unobservable, rendering major questions about how these radiations came to be difficult to tackle. What did the ancestral species of the anole radiation look like? How did new species arise? What processes drove adaptive diversification? Here, we review what we have learned about the cryptic early stages of adaptive radiation from studies of Anolis lizards, and how these studies have attempted to bridge the process-pattern divide of adaptive radiation research. Despite decades of research, however, fundamental questions linking eco-evolutionary processes to macroevolutionary patterns in anoles remain difficult to answer.

Phenotypic Convergence Is Not Mirrored at the Protein Level in a Lizard Adaptive Radiation

Abstract: There are many compelling examples of molecular convergence at individual genes. However, the prevalence and the relative importance of adaptive genome-wide convergence remain largely unknown. Many recent works have reported striking examples of excess genome-wide convergence, but some of these studies have been called into question because of the use of inappropriate null models. Here, we sequenced and compared the genomes of 12 species of anole lizards that have independently converged on suites of adaptive behavioral and morphological traits. Despite extensive searches for a genome-wide signature of molecular convergence, we found no evidence supporting molecular convergence at specific amino acids either at individual genes or at genome-wide comparisons; we also uncovered no evidence supporting an excess of adaptive convergence in the rates of amino acid substitutions within genes. Our findings indicate that comprehensive phenotypic convergence is not mirrored at genome-wide protein-coding levels in anoles, and therefore, that adaptive phenotypic convergence is likely not constrained by the evolution of many specific protein sequences or structures.

Sex-specific microhabitat use is associated with sex-biased thermal physiology in Anolis lizards.

Abstract: If fitness optima for a given trait differ between males and females in a population, sexual dimorphism may evolve. Sex-biased trait variation may affect patterns of habitat use, and if the microhabitats used by each sex have dissimilar microclimates, this can drive sex-specific selection on thermal physiology. Nevertheless, tests of differences between the sexes in thermal physiology are uncommon, and studies linking these differences to microhabitat use or behavior are even rarer. We examined microhabitat use and thermal physiology in two ectothermic congeners that are ecologically similar but differ in their degree of sexual size dimorphism. Brown anoles (Anolis sagrei) exhibit male-biased sexual size dimorphism and live in thermally heterogeneous habitats, whereas slender anoles (Anolis apletophallus) are sexually monomorphic in body size and live in thermally homogeneous habitats. We hypothesized that differences in habitat use between the sexes would drive sexual divergence in thermal physiology in brown anoles, but not slender anoles, because male and female brown anoles may be exposed to divergent microclimates. We found that male and female brown anoles, but not slender anoles, used perches with different thermal characteristics and were sexually dimorphic in thermal tolerance traits. However, field-active body temperatures and behavior in a laboratory thermal arena did not differ between females and males in either species. Our results suggest that sexual dimorphism in thermal physiology can arise from phenotypic plasticity or sex-specific selection on traits that are linked to thermal tolerance, rather than from direct effects of thermal environments experienced by males and females.

An extreme cold event leads to community-wide convergence in lower temperature tolerance in a lizard community.

Abstract: Extreme climate events are predicted to increase in frequency and severity due to contemporary climate change. Recent studies have documented the evolutionary impacts of extreme events on single species, but no studies have yet investigated whether such events can drive community-wide patterns of trait shifts. On 22 January 2020, subtropical south Florida experienced an extreme cold episode during which air temperatures dropped below the lower thermal limit of resident lizard populations. In the week immediately after the cold event, we documented decreased lower thermal limits (CTmin) of six co-occurring lizard species that vary widely in ecology, body size and thermal physiology. Although cold tolerance of these species differed significantly before the cold snap, lizards sampled immediately after had converged on the same new, lower limit of thermal tolerance. Here, we demonstrate that extreme climate events can drive substantial and synchronous community-wide trait changes and provide evidence that tropical and subtropical ectotherms-often characterized as unable to withstand rapid changes in climatic conditions-can endure climatic conditions that exceed their physiological limits. Future studies investigating the mechanisms driving these trait shifts will prove valuable in understanding the ability of ectotherm communities to mitigate climate change.

Recent biological invasion shapes species recognition and aggressive behaviour in a native species: A behavioural experiment using robots in the field.

Abstract: Invasive species are a world-wide threat to biodiversity. Yet, our understanding of biological invasions remains incomplete, partly due to the difficulty of tracking and studying behavioural interactions in recently created species interactions. We tested whether the interactions between the recently introduced invasive lizard Anolis cristatellus and the native Anolis oculatus in Dominica have led to changes in species recognition and aggressive behaviour of the native species. The use of realistic robots allowed us to test the behavioural response of 131 A. oculatus males towards relevant and controlled conspecific versus heterospecific stimuli, directly in the field and in two contexts (allopatry vs. sympatry). Our results show that species recognition evolved prior to sympatry in A. oculatus. Moreover, interspecific competition resulted in an increase in the time spent displaying and a divergence in the aggressive behaviour of the native species towards conspecifics versus heterospecifics. Inherent species recognition and higher aggressive behaviour may limit species coexistence as they are expected to favour A. oculatus during territorial interactions with A. cristatellus. While more studies are needed to understand the causes of these behavioural shifts and their consequences on long-term species coexistence, the present study highlights the role of behaviour as a first response to interspecific interactions.

Eastern Gray Squirrels (Sciurus carolinensis) Differ in Abundance and Response to Humans Across Urban Habitats of St. Louis

Abstract: Behavioral responses to urbanization may differ with environmental variation across metropolitan areas. We compared relative abundance and escape behavior of Sciurus carolinensis (Eastern Gray Squirrels) in common urban habitats in St. Louis, Missouri, USA. We found that squirrels were abundant in urban park, forest, and neighborhood habitats and nearly absent in cemeteries and golf courses. Across all sites, we found abundance was positively associated with anthropogenic habitat modification: more people, impervious surface cover, roads, high intensity developed land use, and less canopy cover. Escape responses also varied across the urban landscape. Flight initiation distance, a metric of risk perception, was least in neighborhood and forest habitats and greatest in park and cemetery habitats. Most squirrels fled by sprinting a short distance and stopping in all habitat types, and those that ran quickly to a refuge tended to have greater flight initiation distances. Squirrels more readily fled in habitats with fewer roads and more residential land use. These findings suggest that responses to urbanization in Eastern Gray Squirrels are heterogeneous within the metropolitan region.

Assessing the effects of genetic divergence and morphology on anolis lizard mating

Abstract: The brown anole (Anolis sagrei) is a widespread neotropical lizard found on many islands in the West Indies as well as the coast of Central America. Across their range, brown anole populations show extensive ecomorphological trait variation and substantial genetic divergence. It is unclear, however, whether this genetic and morphological divergence is indicative of reproductive isolation between populations. We investigated variation in mating behavior across populations by analyzing 4 h of video for each of 234 captive male-female pairs encompassing all 36 possible pairings from six sampled islands. For each pair of individuals, we tested for an association between the occurrence of mating, morphological traits, and genetic relatedness of their populations. We found no support for the hypotheses of ecological divergence, nonecological divergence, or both ecological and nonecological divergence driving premating reproductive isolation in A. sagrei. We did find that males with relatively short heads tend to mate more quickly and hypothesize potential explanations that warrant future investigation.