Global Assessment of Reptile Distributions
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Exploring drivers of viviparity amongst global reptiles

5/10/2022

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Picture Top: Cerastes vipera (a live-bearing viperid snake); bottom: Cerastes cerastes (an egg-laying congener). (Photo: Anna Zimin)
In a recent publication in Global Ecology and Biogeography we (Anna and many others) examined the selective forces that potentially drive the evolution of viviparity (live-bearing) in squamates.
Vertebrates are known for their versatility in reproductive strategies and features. Those, in turn, facilitated their successful expansion across various types of environments worldwide. For instance, the evolution of shelled eggs promoted the expansion of tetrapods into terrestrial habitats, and the retention of eggs inside the parent’s body significantly improved embryo survivability in harsh environmental conditions. Live-bearing (henceforth ‘viviparity’) evolved across all major vertebrate groups, except birds, crocodilians and turtles. Whereas it evolved only once in the mammal history, it is thought to evolve over 100 times independently in squamates (lizards and snakes), with about 20% of their species being viviparous. The prevalence of both egg-laying (oviparity) and viviparity in many squamate clades, and the multiple origins of viviparity, make squamates an excellent model to study the selective forces behind the evolution and biogeography of reproductive modes.
In this study, we aimed to examine most of the common selective forces hypothesized to drive the evolution of viviparity, and the relationship of reproductive mode with body size. Specifically, we tested the predictions that viviparity will be associated with (1) cold climates, (2) unpredictable climates, (3) high elevations (a proxy for hypoxic conditions), and (4) large adult body sizes. In order to do that, we collated a dataset for over 9,000 squamate species (about 80% of non-marine living species), making it the largest-scale study on the subject. Furthermore, because the factors mentioned above may be associated both directly and indirectly (i.e., through another factor) with reproductive mode, we used methods, such as path analysis, that enable to detect and account for such complex relationships.
Our main finding was that viviparity was strongly associated with cold climates, in line with earlier studies. In fact, there are relatively more viviparous than oviparous species in colder climates, and some of the coldest regions occupied by squamates do not include oviparous species at all. Notably, although some warm regions harbor many viviparous species (much more than the coldest climates), such regions usually include even more egg-laying species. The roles of climatic variation and of elevation were found to be less important and not straightforward. Even though the proportions of viviparity at high elevations are higher, elevation probably exerts various selective pressures and influences the prevalence of viviparity primarily through its effect on temperature. Our findings highlight the complexity of processes potentially underlying the evolution of viviparity, but they also provide clear support for low temperatures as selecting for viviparity in squamates.

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Top left: Global richness of viviparous squamate species. Top right: latitudinal variation in richness of viviparous squamate species. Bottom left: Proportion of viviparous squamate species in grid cells. Bottom right: latitudinal variation in proportion of viviparous squamate species.
Author: Anna Zimin
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Modelling IUCN threat status for global reptiles

1/5/2022

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PictureVallarta Mud Turtle (Kinosternon vogti), classified as ‘Critically Endangered’ by the automated assessment method and as not evaluated by the IUCN Red List of Threatened Species (Photo: Agencia Informativa Conacyt/ Wikimedia)
Reptiles comprise nearly 11,800 species worldwide, and are the most species-rich land-vertebrate group. After 18 years of laborious work by many experts globally, early in 2022, the first extinction risk assessment of this group was completed (the Global Reptile Assessment). This important endeavor will enable adding reptiles to global conservation policy and management initiatives as one of the major groups assessed. Nevertheless, this assessment still leaves over 3000 reptile species that have either not been assessed or were assigned a data deficient category that prevents their prioritization for conservation. In an effort to fill-in this gap a new publication in the journal PLOS Biology, we presents estimates of extinction risk for those species currently neglected by the Global Reptile Assessment, using novel machine learning modelling. importantly we found that unassessed and data deficient reptile species are more likely to threatened than assessed species.
Gabriel Caetano, lead author of the paper explained “The IUCN threat assessment procedure is highly important, yet very lengthy, data intensive, subject to human decision biases, and relies on in-person meetings of experts. However, we can use information on already assessed species to better understand the risks to those not yet assessed. Species may share physiological, geographic, and ecological attributes (often via shared evolutionary history) that make them more threatened, and experience similar sources of threat when they occur at similar locations. In our work we tried to emulate the IUCN process using predominantly remotely sensed data and advanced machine learning methods. We used species that have been assessed to teach our models what makes a species threatened and then predict the threat categories of unassessed species”. He added “our new methods are important for highlighting reptile species at risk and can be used on other groups as an initial shortcut for threat categorization”.
Shai Meiri added “Importantly, the additional reptile species identified as threatened by our models are not distributed randomly across the globe or the reptilian evolutionary tree. Our added information highlights that there are more reptile species in peril – especially in Australia, Madagascar, and the Amazon basin – all of which have a high diversity of reptiles and should be targeted for extra conservation effort. Moreover, species rich groups, such as geckos and elapids (cobras, mambas, coral snakes, and others), are probably more threatened than the Global Reptile Assessment currently highlights, these groups should also be the focus of more conservation attention”
Uri Roll mentioned “Our work could be very important in helping the global efforts to prioritize the conservation of species at risk – for example using the IUCN red-list mechanism. Our world is facing a biodiversity crisis, and severe man-made changes to ecosystems and species, yet funds allocated for conservation are very limited. Consequently, it is key that we use these limited funds where they could provide the greatest benefits. Advanced tools- such as those we have employed here, together with accumulating data, could greatly cut the time and cost needed to assess extinction risk, and thus pave the way for more informed conservation decision making”.

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Proportion of reptile species in different threat categories for an Automated Assessment Method and for the IUCN Red List of Threatened Species.
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Between a rock and a hard place – unique rare species face grave dangers due to human action

24/11/2021

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In a recent paper published in the journal Science Advances Gopal explored drivers of phylogenetically endemic land vertebrates. He also looked at conservation attributes of regions with high phylogenetically endemic species.

We live in the age of the ‘sixth mass extinction’. Our daily activities are causing hundreds and thousands of species to be lost forever. To turn the tide on the biodiversity crisis we have to identify those regions and species that are most in need of our conservation efforts. However, the characteristics of regions or species most in need of protection are not always clear. In this work we focus on those species that have two distinct features that make especially good candidates for conservation efforts. First – they are confined to only small and distinct location on the globe – what are known as endemic species and face greater risk of extinction. Second – they are evolutionary unique - they do not have close relatives on the ‘tree of life’ and their loss will represent a loss of millions of years of evolution. Species that poses both of these attributes (phylogenetic endemics) are therefore of great conservation importance as they represent unique and threatened components of biodiversity. To explore these species, we collected data regarding the evolutionary relationships and geographic distribution of almost all land vertebrate species (~30,000 species of amphibians, birds, mammals, and reptiles). We set out to map global ‘hotpots’ of such species, understand what are the unique conditions that support them, and evaluate their current protection and threats.
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Some of the range-restricted evolutionary unique species. The Red ruffed lemur (photo credit: Charles J Sharp), Madagascar fish eagle (photo credit: Anjajavy le Lodge), Hula painted frog (photo credit: Gopal Murali - own image), and Chinese Crocodile Lizard (photo credit: Holger Krisp). Images from Wikimedia Commons (apart from the painted frog).

We found that hotspots of phylogenetically endemic species mostly occur in the tropics and in the southern hemisphere along mountain ranges and in islands. Altogether, these hotspots, when combining the hotspots for all of the four above-mentioned groups, they occupy 22% of the total landmass. Hotspots that were important for all of the four groups are located in the Caribbean islands, Central America, along the Andes, eastern Madagascar, Sri Lanka, southern Western Ghats in India, and New Guinea. Although some of these regions have been previously prioritized for conservation actions, our study also found hotspots outside well-known biodiversity centres. For instance, we found the Asir mountains in Saudi Arabia to be important for such unique birds and Morocco to harbour phylogenetically endemic reptiles. Globally, these regions are mostly defined as mountainous tropical regions. This finding supports the notion that tropical mountains have an important role in the generation and maintenance of biodiversity.

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Global map of Phylogenetic endemism hotspots for all land vertebrates corrected for species richness

We next quantified how human activities and climate change are threatening these hotspots. Alarmingly, we found human activities such as buildings, roads, land-use, population density, and rate of climate change to be disproportionately higher in these hotspots (when compared to regions outside them). Consequently, our study highlights that many uniquely rare species, which probably perform important roles in the ecosystem, will be the first to be lost due to global change. Furthermore, we found most of the hotspots are not adequately protected. About 70% of the hotspots regions have less than 10% overlap with protected areas. Some of these regions which require urgent conservation action are the southern Andes, Horn of Africa, Southern Africa, and the Solomon Islands.
 
To-date most conservation strategies still focus on species-rich regions or flagship species, which may miss out on regions with uniquely rare species we identified. Overall, our study emphasizes on the need for strategic conservation policy and management to safeguard the persistence of thousands of small-ranged species that represent millions of years of unique evolutionary history.

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Infographic representing this work. Press to download in high resolution
Author: Gopal Murali
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What are the intrinsic and extrinsic drivers of lizard clutch-size evolution?

14/6/2020

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In a recent publication in Global Ecology and Biogeography GARDians explored the global diversity and distribution of lizard clutch sizes.
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We tested the geographic factors that affect clutch sizes in across nearly 4000 lizard species. We found similar patterns to those that have long been known in birds but were never seriously studied in other groups of organisms: lizards lay large clutches at high latitudes and at highly seasonal regions. We postulate that high latitudes with their short, pronounced productivity peals both allow the production of large clutches and promote putting all the eggs in one basket – because the window of opportunity is short in highly seasonal regions. We hypothesize that this may further be a factor preventing taxa with fixed clutch sizes from colonizing high latitudes.

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Median log‐transformed clutch size in 96 km × 96 km grid cells globally. Top: all lizards; bottom: only lizards with variable clutch sizes. Note that the colour scale differs between the maps. To the right of each map is a curve showing a generalized additive model of the mapped variable (in black), the 95% confidence intervals of the mapped variable per 96‐km latitudinal band (shaded dark grey), and the range of values of the mapped variable per 96‐km latitudinal band (shaded light grey).
Authors: Shai Meiri, Uri Roll
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No evidence of shorter lifespans for tetrapods with higher metabolism

20/3/2020

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It has long been thought that animals that ‘live slowly’, having a slow rate of metabolism, live longer than those that live their lives at a fast rate: having high metabolic rates. The notion is based on the assumption that animals with fast metabolic rates are more active, more exposed to predators, have higher rates of potentially harmful somatic mutations and produce more harmful metabolic by products such as free radicals. This tradeoff between metabolism and lifespan is commonly referred to as the ‘rate-of-living’ theory.
In a recent publication in the Journal Global Ecology and biogeography, we (Gavin Stark; Daniel Pincheira donoso and Shai Meiri) showed that the assumption under the “rate of living” theory which have been around for almost a century is unsupported by the results of our largest scale study (4,100 land vertebrate species: 2,214 endotherms & 1,886 ectotherms) to date of this theory. We could not find any connection between animal metabolic rate and longevity, either when we tested all land vertebrates (i.e. Mammals, Birds, Reptiles and Amphibians) or when we tested each group separately. In contrast, we did find other factor that did affect the lifespan of ectotherms (Reptiles and Amphibians), and it is ambient temperature. In colder regions around the world we expect species of reptiles and amphibians to live longer than other ectotherms living in warmer environments. The link between ectothermic (amphibians and reptiles) lifespan and ambient temperatures could mean that they are especially vulnerable to the unprecedented global warming that the planet is currently experiencing. Indeed, if increasing ambient temperatures reduces longevity, it may make ectothermic species more prone to go extinct as the climate warms. Our findings add a previously overlooked layer to the range of factors that are commonly thought to imperil species in the Anthropocene.
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The relationship between longevity (y axis of all panels, log10 transformed) and (a–d) body mass (in g, log10 transformed) of amphibians (red circles), reptiles (black circles), birds (green triangles) and mammals (inverted blue triangles). (e–h) Mean annual temperature (regression lines only shown for amphibians and reptiles for which the relationship is significant), (i) basal metabolic rate (in ml O2/hr, log10 transformed), according to the color codes depicted in the top plots and (j) field metabolic rate (kJ/day, log10 transformed)
Author: Gavin Stark
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Nocturnal activity does not prolong gekkotan lifespan

20/3/2020

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In a recent publication in the Israel journal of ecology and evolution, we (Gavin Stark, Rachel Schwarz and Shai Meiri) showed that nocturnality does not prolong lifespan among the within gekkotan species. Species from the infraorder Gekkota are known to be predominately nocturnal as opposed to other lizard clades. Diurnal lizards demonstrate higher metabolic rates than nocturnal ones. Moreover, exposure to solar radiation is thought to reduce ectothermic longevity by increasing both metabolic costs and the rate of accumulating harmful mutations through UV radiation. Thus, we assume that by being nocturnal, ectothermic species may reduce their intrinsic mortality rates and thus live longer. We compared groups of nocturnal and diurnal species across all gekkotan families, and also compared all non-gekkotan species to geckos (740 lizard species, of which 185 are geckos) to test whether nocturnality select for longer lifespans. We found that geckos live relatively long for lizards of their size, however their activity time was found to be unrelated to longevity, contradicting our predictions. We suggest that mortality through extrinsic causes (e.g., predation) may impose much stronger selective pressures than intrinsic causes.
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Mediodactylus kotschyi
Author: Gavin Stark
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Here be dragons; but why? The biogeography and evolution of Melanesian forest dragons (Agamidae)

9/2/2020

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PictureHypsilurus papuensis (Photo Oliver Tallowin)
Australia and New Guinea, collectively referred to as the Sahul, share many biotic elements; but could not be more different in terms of climate and geological history. Australia as a landmass is relatively geologically stable, does not have much in the way of mountains and is predominantly covered in arid deserts. In contrast, New Guinea is relatively young in geological terms, has extensive mountains ranges across the entire island and is largely covered in tropical rainforests. From a biogeographical perspective these landmasses present very different opportunities and challenges to their prospective biotic assemblages, and yet, there are some lineages that have diversified throughout both regions. Agamids, also referred to as ‘dragons’, have proliferated in arid Australia represented by over 100 species and have been relatively well studied. With 20 recognised species, Melanesian agamids are much less diverse, have received much less scientific attention, and yet have been shown to be closely related to the Australian clade. In a paper published in the Biological Journal of the Linnean Society, we examine the evolution, biogeography and ecological diversity of Melanesian agamids. We tested whether they originated on the Australian Craton or proto-Papuan islands to the north. Also, we examined to what extent mountains have played a role in Melanesian agamid diversification and tested the evolutionary trends and origins of agamid ecological diversity.

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α-Diversity of agamids across Australia, New Guinea and surrounding islands
PictureLophosaurus dilophus (Photo Oliver Tallowin)
In addition to the 11 recognised Melanesian agamids sampled, we found further monophyletic divergent lineages in four taxa. This included two lineages within Hypsilurus modestus, and three within H. magnus, H. papuensis and Lophosaurus dilophus. We found little evidence for micro-endemism in Melanesia with most taxa being widespread and low genetic divergence across the Central Cordillera suggesting these mountains have only recently become a barrier to dispersal. We identified clear evidence of past over-water dispersal in Hypsilurus agamids, with H. modestus lineages dispersing between New Britain, New Ireland and northeast New Guinea. Also, the restricted range of H. schoedei and disjunct distribution of H. longii indicates insular extinction events may have occurred. We identify the Australian Craton as the ancestral area of Lophosaurus and all Australo-Papuan agamids. However, Hypsilurus were clearly able to disperse over water and show deep divergences in the Melanesia region. The distribution of extant Hypsilurus lineages suggests a history of allopatric speciation on former islands with some now accreted onto New Guinea. We infer from the biome evolution analysis that Australo-Papuan agamids were associated with rainforests which date back to the early Miocene, but also that agamids had similarly long histories in other biomes. This indicates that while the rainforest biome might well be ancestral for many Australian radiations, semi-arid or seasonal environments also have a long history in Sahul. Finally, we note the disparity in ecological diversity within Australo-Papuan agamids. Despite their long history in rainforest regions there is a complete lack of Melanesian terrestrial or semi-terrestrial agamids compared with the Australian assemblage. This reflects fundamental differences in how these lizards diversify in dry versus wet habitats and suggests adverse environmental conditions, such as reduced solar radiation, as well as biotic interactions, such as competition or predation, form a barrier to ecological diversification in rainforest biomes.

Author: Oliver Tallowin
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Unraveling evolutionary trends in New Guinean geckos

9/2/2020

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Uncovering the evolutionary trajectories of species assemblages can provide fascinating insights into the past environmental and geological processes, as well as the biological traits, that have led to present day diversity patterns. Furthermore, time-calibrated phylogenies can shed light on the historical sequence and timing of speciation events which, in turn, can be used to complement geological models aimed at reconstructing the formation of the earth. In our paper published in Molecular Phylogenetics and Evolution, we focus on the Melanesian radiation of bent-toed geckos (Cyrtodactylus), a clade occurring throughout New Guinea and adjacent islands, and Australia’s tropical northeast. We examine the sequence and timing of diversification in Australo-Papuan Cyrtodactylus and investigated three biogeographic scenarios. Firstly, did Cyrtodactylus diversification originate on the Australian Craton or former proto-Papuan islands to the north. Secondly, does Australo-Papuan Cyrtodactylus diversity correlate with distinct geological regions and to what degree do they exhibit infra-regional clustering. Lastly, to what extent did New Guinea mountain uplift impact Cyrtodactylus diversification and if so when did this occur.
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Cyrtodactylus serratus (Photo S. Richards)
We found that in addition to 28 recognised Australo-Papuan Cyrtodactylus species, there were ten distinct lineages that we consider candidate species. Our ancestral-state analyses support the early origin and diversification of Australo-Papuan Cyrtodactylus on the proto-Papuan islands, and indicate that once insular lineages arrived to New Guinea following the accretion of their associate island onto the mainland’s northern margin. We found a high degree of phylogenetic clustering within the regions and found compelling evidence that the East-Papuan Composite Terrane (or south-eastern Papuan Peninsula) has played a long-term important role in the accumulation of New Guinean Cyrtodactylus. Finally, we identified that the Late-Miocene uplift of New Guineas Central Cordillera was responsible for isolating north-south lineages and mediated the accumulation of diversity in a manner consistent with that observed in other tropical mountain regions.

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Cyrtodactylus epiroticus (Photo Oliver Tallowin)
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Geographic distribution of each of the nine major lineages are illustrated with corresponding colors on the two maps, and specimen representatives of each lineage shown on the right.
Author: Oliver Tallowin
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Viviparity does not affect the numbers and sizes of reptile offspring

25/1/2020

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In a recent publication in the Journal of Animal Ecology we show that the fundamental changes to the mode of life that viviparity brings to squamate females, were surprisingly not reflected in either the number of offspring produced at a single reproductive event (birth, clutch), or their size, or the total mass of offspring produced relative to the size of their mother. The distributions of all these traits in viviparous squamates are remarkably similar to those of oviparous ones. Incidentally we have found that the mass of a recently hatched squamate is (on average, despite much variation) similar to the mass of the egg its mother laid.
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Vipera bornmuelleri on Mt. Hermon (photo Uri Roll)
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Birds and Mammals are not that special (in offspring sizes)

25/1/2020

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In a recently published paper in the Biological Journal of the Linnean Society Shai has shown that the spread of ratios of hatchling or neonate masses to adult masses is very similar across the three classes of amniotes (mammals, birds and, of course, reptiles). This suggests that relatively large offspring are the ancestral and dominant mode of amniotes and have not evolved in response to the elaborate parental care of endotherms
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The relative frequencies of the ratio of offspring size to adult size in mammals (grey), squamates (black) and birds (white). The peak at the smallest ratio is almost entirely composed of metatherians, but mammals (mostly bats) also dominate the highest ratio categories. Note that the range of values is narrower in birds than in either squamates or mammals.
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