There and back again: when and how the world's richest snake family (Dipsadidae) dispersed and speciated across the Neotropical region

Aim The widespread megadiverse Neotropical snake family Dipsadidae occurs in a large range of diverse habitats. Therefore, it represents an excellent model to study the diversification of Neotropical biota. Herein, by generating a time-calibrated species-level phylogeny, we investigate the origin and historical biogeography of Dipsadidae and test if its two main Neotropical subfamilies, Xenodontinae and Dipsadinae, have different geographical origins. Location Neotropical region. Taxon Dipsadidae (Serpentes). Methods We generated a new Bayesian time-calibrated phylogeny based on published sequences from six genes for 344 species, including 287 species of Dipsadidae. We subsequently estimated ancestral areas of distribution by comparing models in BioGeoBEARS: DEC (subset sympatry, narrow vicariance), DIVALIKE (narrow and wide vicariance), BAYAREALIKE (no vicariance and widespread sympatry), also testing jump dispersal. We also estimated shifts in the diversification of this group using BAMM, exploring possible relationships with its historical biogeography. Results The best models show that Dipsadidae likely originated approximately 50 million years ago (mya) in Asia. Dispersal was a fundamental process in its historical biogeography. The DEC model with jump dispersal indicated that this family underwent a range extension from Asia and posterior vicariance of North and Central America ancestors. Both Xenodontinae and Dipsadinae originated in Central America and dispersed to South America during Middle Eocene, but did so to different regions (cis and trans-Andean South America, respectively). Xenodontinae entered cis-Andean South America around 39 mya and jump dispersed to the West Indies around 33 mya, while Dipsadinae entered trans-Andean South America multiple times 20–38 mya. The diversification rate decreased through time, except for a clade within Dipsadinae composed of the Dipsadini tribe and the Atractus and Geophis genera. Main Conclusions Our results show that Dipsadidae has an Asian origin and that the two main Neotropical subfamilies originated in Central America, later dispersing to South America in different time periods. This difference is also reflected in the higher diversification rate for the ‘goo-eaters’ in the Dipsadinae subfamily. The current biogeographical patterns of the family Dipsadidae, the most species-rich snake family in the world, have likely been shaped by complex evolutionary and geological processes such as Eocene land bridges, Andean uplift and the formation of the Panama isthmus.

Reproductive and environmental traits explain the variation in egg size among Medusozoa (Cnidaria).

Medusozoa (Cnidaria) are characterized by diverse life cycles, with different semaphoronts (medusa, medusoid, fixed gonophore, polyp) representing the sexual phase and carrying the gametes. Although egg size is often considered a proxy to understand reproductive and developmental traits of medusozoans, understanding of the processes influencing egg size variation in the group under an evolutionary context is still limited. We carried out a comprehensive review of the variation of egg size in Medusozoa to test whether this variation is related to biological/sexual or environmental traits. Egg size presents a strong phylogenetic signal (λ = 0.79, K = 0.67), explaining why closely related species with different reproductive strategies and different individual sizes have similar egg sizes. However, variation in egg size is influenced by the number of eggs, depth and temperature, with larger eggs frequently present in species with few eggs (1-15), in deep-sea species and in cold-water species. Conversely, the production of small eggs among cold-water species of Staurozoa might be associated with the development of a small benthic larvae in this group. Our study reinforces that egg sizes respond to reproductive and environmental traits, although egg size is highly conserved within medusa classes.

Finding love in a hopeless place: A global database of misdirected amplexus in anurans.

Amphibians are one of the most species-rich vertebrate taxa, with diverse and complex reproductive behaviors. Even though mate recognition plays a vital role in reproductive success, unusual amplexus with non-suitable mates (misdirected amplexus) have been reported to occur in the wild. Misdirected amplexus may decrease fitness, thus likely having ecological and evolutionary consequences and their frequency might increase with human-induced changes in habitat. However, it is still unclear what promotes this unusual behavior and how widespread it is at spatial and phylogenetic scales. To fill this gap, we compiled a global database of misdirected amplexus events from literature and personal observations, with detailed information on environmental, geographical, and behavioral aspects of reported events. Furthermore, we discuss its spatial, temporal, and phylogenetic patterns. We provide a data set of 378 misdirected amplexus events for 156 amplectant species distributed across 69 genera and 18 families distributed in 52 countries in all continents except Antarctica. We collected data published or collected during the last 100 years, from 1920 to 2020, with information on the hour, month, and year of the misdirected amplexus events. We recorded a total of 282 interspecific amplexus, 46 necrophiliac amplexus, and 50 amplexus with objects or non-amphibian species, with the United States and Brazil being the countries with the highest number of records. Misdirected amplexus did not occur equally in all zoogeographical realms, with most events occurring in the Neotropical and Nearctic realms. Interspecific amplexus was especially represented in the Neotropical and Mediterranean regions. Most events involved three species-rich globally distributed families (Bufonidae, Ranidae, and Hylidae) but misdirected amplexus was widespread in the phylogeny. We provide a comprehensive data set of misdirected amplexus for anurans, with our results showing that it occurs extensively in the wild and across the globe. This data set provides a baseline for understanding misdirected amplexus and their spatial, temporal, and phylogenetic patterns. Likewise, this data set offers a baseline to test the environmental, ecological, and ethological drivers behind this reproductive behavior and we encourage researchers to report detailed observations of misdirected amplexus to better understand this process and its potential costs at the individual and population levels. The data are not copyright restricted; this data paper should be cited when data are used for publication, and the authors would appreciate being notified of research projects or teaching purposes when these data are used.

Linking body condition and thermal physiology in limping crickets: Does limb autotomy incur costs concerning behavioral thermal tolerance?

Many ectotherms have the ability to voluntarily detach a body part, known as autotomy, usually in response to predator attacks. Autotomy can have an immediate benefit for survival, but it can also involve costs related to the individual's body condition. Even though the effects of autotomy have been studied in many ecophysiological aspects, its short-term costs on the ability to tolerate high environmental temperatures are still unexplored. Herein, we evaluated the effects of autotomy on the behavioral thermal tolerance (VTMax ) in the cricket Gryllus assimilis. We hypothesized that, due to the increased energetic costs to maintain homeostasis, autotomized crickets have a lower VTMax than intact ones. Additionally, we investigated differences in VTMax between sexes, as well as the effects of heating rates and body mass on their VTMax . Contrary to our hypothesis, we found no differences between VTMax of autotomized and intact individuals. However, we observed that females have a higher VTMax than males, regardless of their condition (i.e., autotomized and intact). Moreover, we detected significant effects of body mass and heating rate on behavioral thermal tolerances. The results of our study indicate that costs associated with limb autotomy at high environmental temperatures might be intricate and not immediately impactful. Furthermore, important aspects of reproduction and ecology might be responsible for differences in VTMax between males and females. Our results contribute to understanding the ecological and physiological aspects of ectotherms and how they respond to changing climatic conditions.

VTMaxHerp: A data set of voluntary thermal maximum temperatures of amphibians and reptiles from two Brazilian hotspots.

Amphibians and reptiles are ectothermic animals and therefore depend on environmental temperatures to maintain their physiological functions. Despite being poorly documented, data on thermal behavioral thresholds to avoid overheating in their habitats are essential to improve the understanding of their thermal ecology and physiology. Here we provide a data set of 312 individual voluntary thermal maximum (VTMax ) values, the maximum temperature tolerated by individuals before actively moving to a colder place, for 53 species of amphibians and reptiles of the Atlantic Forest and Cerrado savannas of southeastern South America. Voluntary thermal maximum values were recorded as the body temperature at which the individuals exited a heating box experimental setup. This data set comprises 25 species of 15 genera and eight families of amphibians and 28 species of 24 genera and 12 families of reptiles. Of the total number of individual records, 67.9% derived from the Cerrado and 32.0% derived from the Atlantic Forest ecoregions. Overall, lizards had higher VTMax than amphibians and snakes, and individuals in the Atlantic Forest had overall higher VTMax values than the ones in Cerrado. This data set is the first to compile VTMax values for South American herpetofauna, along with detailed experimental information such as heating rates and time to reach VTMax . This data set provides a baseline for understanding thermal tolerances and requirements of Neotropical ectothermic vertebrate species, which might be useful for future research on the impact of climate change and to test novel ecological hypotheses. There are no copyright or proprietary restrictions except that this data paper should be cited when data are used for publications. In addition, the authors would appreciated being informed of research projects or teaching purposes when these data are used.

Linking body condition and thermal physiology in limping crickets: does limb autotomy incur costs concerning behavioral thermal tolerance?

Many ectotherms have the ability to voluntarily detach a body part, known as autotomy, usually in response to predator attacks. Autotomy can have an immediate benefit for survival, but it can also involve costs related to the individual's body condition. Even though the effects of autotomy have been studied in many ecophysiological aspects, its short-term costs on the ability to tolerate high environmental temperatures are still unexplored. Herein, we evaluated the effects of autotomy on the behavioral thermal tolerance (VTMax) in the cricket Gryllus assimilis. We hypothesized that, due to the increased energetic costs to maintain homeostasis, autotomized crickets have a lower VTMax than intact ones. Additionally, we investigated differences in VTMax between sexes, as well as the effects of heating rates and body mass on their VTMax. Contrary to our hypothesis, we found no differences between VTMax of autotomized and intact individuals. However, we observed that females have a higher VTMax than males, regardless of their condition (i.e., autotomized and intact). Moreover, we detected significant effects of body mass and heating rate on behavioral thermal tolerances. The results of our study indicate that costs associated with limb autotomy at high environmental temperatures might be intricate and not immediately impactful. Furthermore, important aspects of reproduction and ecology might be responsible for differences in VTMax between males and females. Our results contribute to understanding the ecological and physiological aspects of ectotherms and how they respond to changing climatic conditions.

Correction: Does behavioral thermal tolerance predict distribution pattern and habitat use in two sympatric Neotropical frogs?

[This corrects the article DOI: 10.1371/journal.pone.0239485.].

Short-term captivity does not affect immediate voluntary thermal maximum of a neotropical pitviper: Implications for behavioral thermoregulation.

Ectotherms depend on temperature to maintain their physiological functions and through behavioral changes, they can avoid overheating in their habitats. The voluntary thermal maximum (VTMax ) represents the maximum temperature tolerated by individuals before actively moving to a colder place. However, if and how VTMax might change after capture and in captivity remains understudied. We investigate if measurements taken in captivity are a good proxy for thermal tolerance of wild individuals. As thermal history has been shown to affect behavioral response and physiological parameters, herein we hypothesized that VTMax of the neotropical viper Bothrops pauloensis varies throughout the captivity period. We measured the VTMax of individuals immediately after capture and in three trials during a short-term period in captivity. Measurements were done by recording their body temperature at which they exited a heating box experimental setup. In contrast to our hypothesis, the VTMax was not significantly affected by time in captivity but there was interindividual variation. There were also no significant differences between field and captivity measurements, in spite of the small effect size. Our results indicate that the VTMax of this snake population is not affected by a short-term captivity period. Furthermore, an invariant VTMax might indicate low phenotypic plasticity, as individuals do not appear to adjust their tolerance to short-term exposure to higher temperatures and potential vulnerability to threats such as global warming. We expect that our results can contribute to understanding the effect of captivity on thermal tolerance in neotropical squamates, allowing for insights into their thermal physiology and ecology.

No one-size-fits-all solution to clean GBIF.

Species occurrence records provide the basis for many biodiversity studies. They derive from georeferenced specimens deposited in natural history collections and visual observations, such as those obtained through various mobile applications. Given the rapid increase in availability of such data, the control of quality and accuracy constitutes a particular concern. Automatic filtering is a scalable and reproducible means to identify potentially problematic records and tailor datasets from public databases such as the Global Biodiversity Information Facility (GBIF; http://www.gbif.org), for biodiversity analyses. However, it is unclear how much data may be lost by filtering, whether the same filters should be applied across all taxonomic groups, and what the effect of filtering is on common downstream analyses. Here, we evaluate the effect of 13 recently proposed filters on the inference of species richness patterns and automated conservation assessments for 18 Neotropical taxa, including terrestrial and marine animals, fungi, and plants downloaded from GBIF. We find that a total of 44.3% of the records are potentially problematic, with large variation across taxonomic groups (25-90%). A small fraction of records was identified as erroneous in the strict sense (4.2%), and a much larger proportion as unfit for most downstream analyses (41.7%). Filters of duplicated information, collection year, and basis of record, as well as coordinates in urban areas, or for terrestrial taxa in the sea or marine taxa on land, have the greatest effect. Automated filtering can help in identifying problematic records, but requires customization of which tests and thresholds should be applied to the taxonomic group and geographic area under focus. Our results stress the importance of thorough recording and exploration of the meta-data associated with species records for biodiversity research.

Does behavioral thermal tolerance predict distribution pattern and habitat use in two sympatric Neotropical frogs?

Environmental temperatures are a major constraint on ectotherm abundance, influencing their distribution and natural history. Comparing thermal tolerances with environmental temperatures is a simple way to estimate thermal constraints on species distributions. We investigate the potential effects of behavioral thermal tolerance (i. e. Voluntary Thermal Maximum, VTMax) on anuran local (habitat) and regional distribution patterns and associated behavioral responses. We tested for differences in Voluntary Thermal Maximum (VTMax) of two sympatric frog species of the genus Physalaemus in the Cerrado. We mapped the difference between VTMax and maximum daily temperature (VTMax-ETMax) and compared the abundance in open and non-open habitats for both species. Physalaemus nattereri had a significantly higher VTMax than P. cuvieri. For P. nattereri, the model including only period of day was chosen as the best to explain variation in the VTMax while for P. cuvieri, the null model was the best model. At the regional scale, VTMax-ETMax values were significantly different between species, with P. nattereri mostly found in localities with maximum temperatures below its VTMax and P. cuvieri showing the reverse pattern. Regarding habitat use, P. cuvieri was in general more abundant in open than in non-open habitats, whereas P. nattereri was similarly abundant in these habitats. This difference seems to reflect their distribution patterns: P. cuvieri is more abundant in open and warmer habitats and occurs mostly in warmer areas in relation to its VTMax, whereas P. nattereri tends to be abundant in both open and non-open (and cooler) areas and occurs mostly in cooler areas regarding its VTMax. Our study indicates that differences in behavioral thermal tolerance may be important in shaping local and regional distribution patterns. Furthermore, small-scale habitat use might reveal a link between behavioral thermal tolerance and natural history strategies.

Atlas of Brazilian snakes: verified point-locality maps to mitigate the wallacean shortfall in a megadiverse snake fauna

Accurate and detailed species distribution maps are fundamental for documenting and interpreting biological diversity. For snakes, an ecologically diverse group of reptiles, syntheses and detailed data on distribution patterns remain scarce. We present the first comprehensive collection of detailed, voucher-based, point-locality, range maps for all described and documented Brazilian snakes, with the major aim of mitigating the Wallacean shortfall and as a contribution towards a better understanding of this rich, threatened, and poorly studied megadiverse fauna. We recorded a total of 412 snake species in Brazil on the basis of an extensive and verified point-locality database of 163,498 entries and 75,681 unique records (available here as Online Supporting Information). Our results reveal previously undocumented patterns of distribution, sampling effort, richness, and endemism levels, resulting in a more objective view of snake diversity in the Neotropics. Apart from these achievements, we understand that the most relevant and enduring contribution of the present atlas is to stimulate researchers to publish corrections, additions, and new discoveries.

Atlas of Brazilian snakes: verified point-locality maps to mitigate the wallacean shortfall in a megadiverse snake fauna

Accurate and detailed species distribution maps are fundamental for documenting and interpreting biological diversity. For snakes, an ecologically diverse group of reptiles, syntheses and detailed data on distribution patterns remain scarce. We present the first comprehensive collection of detailed, voucher-based, point-locality, range maps for all described and documented Brazilian snakes, with the major aim of mitigating the Wallacean shortfall and as a contribution towards a better understanding of this rich, threatened, and poorly studied megadiverse fauna. We recorded a total of 412 snake species in Brazil on the basis of an extensive and verified point-locality database of 163,498 entries and 75,681 unique records (available here as Online Supporting Information). Our results reveal previously undocumented patterns of distribution, sampling effort, richness, and endemism levels, resulting in a more objective view of snake diversity in the Neotropics. Apart from these achievements, we understand that the most relevant and enduring contribution of the present atlas is to stimulate researchers to publish corrections, additions, and new discoveries.