Sex determination,longevity, and the birth and death of reptilian species

Vertebrate sex‐determining mechanisms (SDMs) are triggered by the genotype (GSD), by temperature (TSD), or occasionally, by both. The causes and consequences of SDM diversity remain enigmatic. Theory predicts SDM effects on species diversification, and life‐span effects on SDM evolutionary turnover. Yet, evidence is conflicting in clades with labile SDMs, such as reptiles. Here, we investigate whether SDM is associated with diversification in turtles and lizards, and whether alterative factors, such as lifespan's effect on transition rates, could explain the relative prevalence of SDMs in turtles and lizards (including and excluding snakes). We assembled a comprehensive dataset of SDM states for squamates and turtles and leveraged large phylogenies for these two groups. We found no evidence that SDMs affect turtle, squamate, or lizard diversification. However, SDM transition rates differ between groups. In lizards TSD‐to‐GSD surpass GSD‐to‐TSD transitions, explaining the predominance of GSD lizards in nature. SDM transitions are fewer in turtles and the rates are similar to each other (TSD‐to‐GSD equals GSD‐to‐TSD), which, coupled with TSD ancestry, could explain TSD's predominance in turtles. These contrasting patterns can be explained by differences in life history. Namely, our data support the notion that in general, shorter lizard lifespan renders TSD detrimental favoring GSD evolution in squamates, whereas turtle longevity permits TSD retention. Thus, based on the macro‐evolutionary evidence we uncovered, we hypothesize that turtles and lizards followed different evolutionary trajectories with respect to SDM, likely mediated by differences in lifespan. Combined, our findings revealed a complex evolutionary interplay between SDMs and life histories that warrants further research that should make use of expanded datasets on unexamined taxa to enable more conclusive analyses.     

Turtle mating patterns buffer against disruptive effects of climate change

For organisms with temperature-dependent sex determination (TSD), skewed offspring sex ratios are common. However, climate warming poses the unique threat of producing extreme sex ratio biases that could ultimately lead to population extinctions. In marine turtles, highly female-skewed hatchling sex ratios already occur and predicted increases in global temperatures are expected to exacerbate this trend, unless species can adapt. However, it is not known whether offspring sex ratios persist into adulthood, or whether variation in male mating success intensifies the impact of a shortage of males on effective population size. Here, we use parentage analysis to show that in a rookery of the endangered green turtle (Chelonia mydas), despite an offspring sex ratio of 95 per cent females, there were at least 1.4 reproductive males to every breeding female. Our results suggest that male reproductive intervals may be shorter than the 2-4 years typical for females, and/or that males move between aggregations of receptive females, an inference supported by our satellite tracking, which shows that male turtles may visit multiple rookeries. We suggest that male mating patterns have the potential to buffer the disruptive effects of climate change on marine turtle populations, many of which are already seriously threatened.     

The ecology and evolution of temperature‐dependent reaction norms for sex determination in reptiles: a mechanistic conceptual model

Sex‐determining mechanisms are broadly categorised as being based on either genetic or environmental factors. Vertebrate sex determination exhibits remarkable diversity but displays distinct phylogenetic patterns. While all eutherian mammals possess XY male heterogamety and female heterogamety (ZW) is ubiquitous in birds, poikilothermic vertebrates (fish, amphibians and reptiles) exhibit multiple genetic sex‐determination (GSD) systems as well as environmental sex determination (ESD). Temperature is the factor controlling ESD in reptiles and temperature‐dependent sex determination (TSD) in reptiles has become a focal point in the study of this phenomenon. Current patterns of climate change may cause detrimental skews in the population sex ratios of reptiles exhibiting TSD. Understanding the patterns of variation, both within and among populations and linking such patterns with the selection processes they are associated with, is the central challenge of research aimed at predicting the capacity of populations to adapt to novel conditions. Here we present a conceptual model that innovates by defining an individual reaction norm for sex determination as a range of incubation temperatures. By deconstructing individual reaction norms for TSD and revealing their underlying interacting elements, we offer a conceptual solution that explains how variation among individual reaction norms can be inferred from the pattern of population reaction norms. The model also links environmental variation with the different patterns of TSD and describes the processes from which they may arise. Specific climate scenarios are singled out as eco‐evolutionary traps that may lead to demographic extinction or a transition to either male or female heterogametic GSD. We describe how the conceptual principles can be applied to interpret TSD data and to explain the adaptive capacity of TSD to climate change as well as its limits and the potential applications for conservation and management programs.     

Climate change overruns resilience conferred by temperature‐dependent sex determination in sea turtles and threatens their survival

Temperature‐dependent sex determination (TSD) is the predominant form of environmental sex determination (ESD) in reptiles, but the adaptive significance of TSD in this group remains unclear. Additionally, the viability of species with TSD may be compromised as climate gets warmer. We simulated population responses in a turtle with TSD to increasing nest temperatures and compared the results to those of a virtual population with genotypic sex determination (GSD) and fixed sex ratios. Then, we assessed the effectiveness of TSD as a mechanism to maintain populations under climate change scenarios. TSD populations were more resilient to increased nest temperatures and mitigated the negative effects of high temperatures by increasing production of female offspring and therefore, future fecundity. That buffered the negative effect of temperature on the population growth. TSD provides an evolutionary advantage to sea turtles. However, this mechanism was only effective over a range of temperatures and will become inefficient as temperatures rise to levels projected by current climate change models. Projected global warming threatens survival of sea turtles, and the IPCC high gas concentration scenario may result in extirpation of the studied population in 50 years.     

Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change

Background

In gonochoristic vertebrates, sex determination mechanisms can be classified as genotypic (GSD) or temperature-dependent (TSD). Some cases of TSD in fish have been questioned, but the prevalent view is that TSD is very common in this group of animals, with three different response patterns to temperature.

Methodology/Principal Findings

We analyzed field and laboratory data for the 59 fish species where TSD has been explicitly or implicitly claimed so far. For each species, we compiled data on the presence or absence of sex chromosomes and determined if the sex ratio response was obtained within temperatures that the species experiences in the wild. If so, we studied whether this response was statistically significant. We found evidence that many cases of observed sex ratio shifts in response to temperature reveal thermal alterations of an otherwise predominately GSD mechanism rather than the presence of TSD. We also show that in those fish species that actually have TSD, sex ratio response to increasing temperatures invariably results in highly male-biased sex ratios, and that even small changes of just 1–2°C can significantly alter the sex ratio from 1∶1 (males∶females) up to 3∶1 in both freshwater and marine species.

Conclusions/Significance

We demonstrate that TSD in fish is far less widespread than currently believed, suggesting that TSD is clearly the exception in fish sex determination. Further, species with TSD exhibit only one general sex ratio response pattern to temperature. However, the viability of some fish populations with TSD can be compromised through alterations in their sex ratios as a response to temperature fluctuations of the magnitude predicted by climate change.     

Under what conditions do climate‐driven sex ratios enhance versus diminish population persistence?

For many species of reptile, crucial demographic parameters such as embryonic survival and individual sex (male or female) depend on ambient temperature during incubation. While much has been made of the role of climate on offspring sex ratios in species with temperature‐dependent sex determination (TSD), the impact of variable sex ratio on populations is likely to depend on how limiting male numbers are to female fecundity in female‐biased populations, and whether a climatic effect on embryonic survival overwhelms or interacts with sex ratio. To examine the sensitivity of populations to these interacting factors, we developed a generalized model to explore the effects of embryonic survival, hatchling sex ratio, and the interaction between these, on population size and persistence while varying the levels of male limitation. Populations with TSD reached a greater maximum number of females compared to populations with GSD, although this was often associated with a narrower range of persistence. When survival depended on temperature, TSD populations persisted over a greater range of temperatures than GSD populations. This benefit of TSD was greatly reduced by even modest male limitation, indicating very strong importance of this largely unmeasured biologic factor. Finally, when males were not limiting, a steep relationship between sex ratio and temperature favoured population persistence across a wider range of climates compared to the shallower relationships. The opposite was true when males were limiting – shallow relationships between sex ratio and temperature allowed greater persistence. The results highlight that, if we are to predict the response of populations with TSD to climate change, it is imperative to 1) accurately quantify the extent to which male abundance limits female fecundity, and 2) measure how sex ratios and peak survival coincide over climate.     

Avian-like breathing mechanics in maniraptoran dinosaurs

In 1868 Thomas Huxley first proposed that dinosaurs were the direct ancestors of birds and subsequent analyses have identified a suite of 'avian' characteristics in theropod dinosaurs. Ossified uncinate processes are found in most species of extant birds and also occur in extinct non-avian maniraptoran dinosaurs. Their presence in these dinosaurs represents another morphological character linking them to Aves, and further supports the presence of an avian-like air-sac respiratory system in theropod dinosaurs, prior to the evolution of flight. Here we report a phylogenetic analysis of the presence of uncinate processes in Aves and non-avian maniraptoran dinosaurs indicating that these were homologous structures. Furthermore, recent work on Canada geese has demonstrated that uncinate processes are integral to the mechanics of avian ventilation, facilitating both inspiration and expiration. In extant birds, uncinate processes function to increase the mechanical advantage for movements of the ribs and sternum during respiration. Our study presents a mechanism whereby uncinate processes, in conjunction with lateral and ventral movements of the sternum and gastral basket, affected avian-like breathing mechanics in extinct non-avian maniraptoran dinosaurs.     

Nest-site selection in two eublepharid gecko species with temperature-dependent sex determination and one with genotypic sex determination

At present, most turtles, all crocodilians, and several lizards are known to have temperature-dependent sex determination (TSD). Due to the dependence of sex determination on incubation temperature, the long-term survival of TSD species may be jeopardized by global climate changes. The current study was designed to assess the degree to which this concern is justified by examining nest-site selection in two species of Pattern II TSD geckos (Eublepharis macularius and Hemitheconyx caudicinctus) and comparing these preferences with those of a species with genotypic sex determination (GSD) (Coleonyx mitratus). Temperature preferences for nest sites were found to be both species-specific and female-specific. While H. caudicinctus females selected a mean nest-site temperature (32.4°) very close to the upper pivotal temperature (32°C) for the species, E. macularius females selected a mean nest-site temperature (28.7°C) well below this species' lower pivotal temperature (30.5°C). Thus, the resultant sex ratios are expected to differ between these two TSD species. Additionally, nest-site temperatures for the GSD species were significantly more variable (SE=+0.37) than were temperatures for either of the TSD species (E. macularius SE=±0.10; H. caudicinctus SE =+ 0.17), diereby further demonstrating temperature preferences within the TSD species.     

Body Size Distribution of the Dinosaurs

The distribution of species body size is critically important for determining resource use within a group or clade. It is widely known that non-avian dinosaurs were the largest creatures to roam the Earth. There is, however, little understanding of how maximum species body size was distributed among the dinosaurs. Do they share a similar distribution to modern day vertebrate groups in spite of their large size, or did they exhibit fundamentally different distributions due to unique evolutionary pressures and adaptations? Here, we address this question by comparing the distribution of maximum species body size for dinosaurs to an extensive set of extant and extinct vertebrate groups. We also examine the body size distribution of dinosaurs by various sub-groups, time periods and formations. We find that dinosaurs exhibit a strong skew towards larger species, in direct contrast to modern day vertebrates. This pattern is not solely an artefact of bias in the fossil record, as demonstrated by contrasting distributions in two major extinct groups and supports the hypothesis that dinosaurs exhibited a fundamentally different life history strategy to other terrestrial vertebrates. A disparity in the size distribution of the herbivorous Ornithischia and Sauropodomorpha and the largely carnivorous Theropoda suggests that this pattern may have been a product of a divergence in evolutionary strategies: herbivorous dinosaurs rapidly evolved large size to escape predation by carnivores and maximise digestive efficiency; carnivores had sufficient resources among juvenile dinosaurs and non-dinosaurian prey to achieve optimal success at smaller body size.     

Temperature dependent sex determination and climate change

One possible response of species to climate change is shifting their geographical range so as to track their climatic niche. Many concerns have been raised about the species ability to disperse effectively. I argue that species may have mechanisms, like temperature-dependent sex determination (TSD), that are responsive to climate change and may facilitate an appropriate shift in their geographical range. More specifically, I hypothesize that, under stable climatic conditions, populations of some TSD species at the edge of their range are regulated by reduced growth rate (due to skewed sex ratios or due to limited availability of suitable nesting sites). Under climate change, these populations face new climatic conditions that trigger fast population growth (e.g. by more balanced sex ratio, or greater availability of nesting sites). Increased population size may lead to increased dispersal, and thus efficient colonization of the newly created habitat patches. So, the species rapidly tracks the geographical position of its climatic niche. This conceptual model is speculative but it leads to specific hypotheses, and opens up new research questions about the existence of prior adaptations that will enable the appropriate response to climate change.     

Pattern and scale of geographic variation in environmental sex determination in the Atlantic silverside,Menidia menidia

The Atlantic silverside, Menidia menidia (Pisces: Atherinidae), exhibits an exceptionally high level of clinal variation in sex determination across its geographic range. Previous work suggested linear changes in the level of temperature‐dependent sex determination (TSD) with increasing latitude. Based on comparisons at 31 sites encompassing the entire species’ range, we find that the change in level of TSD with latitude is instead highly nonlinear. The level of TSD is uniformly high in the south (Florida to New Jersey), then declines rapidly into the northern Gulf of Maine where genotypic sex determination (GSD) predominates and then rebounds to moderate levels of TSD in the northern‐most populations of the Gulf of St. Lawrence. Major latitudinal breakpoints occur in central New Jersey (40^oN) and the northern Gulf of Maine (44^oN). No populations display pure TSD or GSD. Length of the growing season is the likely agent of selection driving variation in TSD with a threshold at 210 days. Because gene flow among populations is high, such distinct patterns of geographic variation in TSD/GSD are likely maintained by contemporary selection thereby demonstrating the adaptive fine tuning of sex determining mechanisms.     

Novel evolutionary pathways of sex‐determining mechanisms

Evolutionary transitions between sex‐determining mechanisms (SDMs) are an enigma. Among vertebrates, individual sex (male or female) is primarily determined by either genes (genotypic sex determination, GSD) or embryonic incubation temperature (temperature‐dependent sex determination, TSD), and these mechanisms have undergone repeated evolutionary transitions. Despite this evolutionary lability, transitions from GSD (i.e. from male heterogamety, XX/XY, or female heterogamety, ZZ/ZW) to TSD are an evolutionary conundrum, as they appear to require crossing a fitness valley arising from the production of genotypes with reduced viability owing to being homogametic for degenerated sex chromosomes (YY or WW individuals). Moreover, it is unclear whether alternative (e.g. mixed) forms of sex determination can persist across evolutionary time. It has previously been suggested that transitions would be easy if temperature‐dependent sex reversal (e.g. XX male or XY female) was asymmetrical, occurring only in the homogametic sex. However, only recently has a mechanistic model of sex determination emerged that may allow such asymmetrical sex reversal. We demonstrate that selection for TSD in a realistic sex‐determining system can readily drive evolutionary transitions from GSD to TSD that do not require the production of YY or WW individuals. In XX/XY systems, sex reversal (female to male) occurs in a portion of the XX individuals only, leading to the loss of the Y allele (or chromosome) from the population as XX individuals mate with each other. The outcome is a population of XX individuals whose sex is determined by incubation temperature (TSD). Moreover, our model reveals a novel evolutionarily stable state representing a mixed‐mechanism system that has not been revealed by previous approaches. This study solves two long‐standing puzzles of the evolution of sex‐determining mechanisms by illuminating the evolutionary pathways and endpoints.     

Evolution of sex chromosomes in Sauropsida

Reptiles (sauropsids) represent the sister group to mammals, and the basal members of Reptilia may provide a good model for the condition of the common ancestor of both groups. Sex-determining mechanisms (SDM) and organizations of sex chromosomes among genotypically sex-determining (GSD) species vary widely across reptiles. Birds and snakes, for example, are entirely GSD whereas other reptiles, like all crocodilians, exhibit temperature-dependent sex determination (TSD). Here we explore the evolution of sex chromosomes and SDM within reptiles, using family-level analyses of character evolution and applying parsimony, likelihood, Bayesian, and stochastic methods. We find support for the common ancestor of amphisbaenians and whiptail lizards (Laterata) possessing the XY (male heterogametic) GSD mechanism, while the ancestors of Testudines and Crocodylia, as well as the larger group Archosauromorpha (here containing turtles) are inferred to have exhibited TSD. We also find evidence consistent with the hypothesis that the XY system is more labile and evolves faster than does the ZW (female heterogametic) system. Phylogenetic-based speciation tests do not support an association between GSD and speciation, and reject the hypothesis that the presence of the XY system is associated with speciation in reptiles.     

Impacts of climate warming and habitat loss on extinctions at species' low-latitude range boundaries

Polewards expansions of species' distributions have been attributed to climate warming, but evidence for climate‐driven local extinctions at warm (low latitude/elevation) boundaries is equivocal. We surveyed the four species of butterflies that reach their southern limits in Britain. We visited 421 sites where the species had been recorded previously to determine whether recent extinctions were primarily due to climate or habitat changes. Coenonympha tullia had become extinct at 52% of study sites and all losses were associated with habitat degradation. Aricia artaxerxes was extinct from 50% of sites, with approximately one‐third to half of extinctions associated with climate‐related factors and the remainder with habitat loss. For Erebia aethiops (extinct from 24% of sites), approximately a quarter of the extinctions were associated with habitat and three‐quarters with climate. For Erebia epiphron, extinctions (37% of sites) were attributed mainly to climate with almost no habitat effects. For the three species affected by climate, range boundaries retracted 70–100 km northwards (A. artaxerxes, E. aethiops) and 130–150 m uphill (E. epiphron) in the sample of sites analysed. These shifts are consistent with estimated latitudinal and elevational temperature shifts of 88 km northwards and 98 m uphill over the 19‐year study period. These results suggest that the southern/warm range margins of some species are as sensitive to climate change as are northern/cool margins. Our data indicate that climate warming has been of comparable importance to habitat loss in driving local extinctions of northern species over the past few decades; future climate warming is likely to jeopardize the long‐term survival of many northern and mountain species.     

Temperature-Dependent Sex Determination in Sea Turtles in the Context of Climate Change: Uncovering the Adaptive Significance

The adaptive significance of temperature-dependent sex determination (TSD) in reptiles remains unknown decades after TSD was first identified in this group. Concurrently, there is growing concern about the effect that rising temperatures may have on species with TSD, potentially producing extremely biased sex ratios or offspring of only one sex. The current state-of the-art in TSD research on sea turtles is reviewed here and, against current paradigm, it is proposed that TSD provides an advantage under warming climates. By means of coadaptation between early survival and sex ratios, sea turtles are able to maintain populations. When offspring survival declines at high temperatures, the sex that increases future fecundity (females) is produced, increasing resilience to climate warming. TSD could have helped reptiles to survive mass extinctions in the past via this model. Flaws in research on sex determination in sea turtles are also identified and it is suggested that the development of new techniques will revolutionize the field.     

Relic thermosensitive gene expression in a turtle with genotypic sex determination

The evolution of sex determination remains one of the most fascinating enigmas in biology. Transitions between genotypic sex determination (GSD) and temperature‐dependent sex determination (TSD) have occurred multiple times during vertebrate evolution, however, the molecular basis and consequences of these transitions in closely related taxa remain unresolved. Here I address a critical question: Do species with GSD derived from ancestors possessing TSD retain any ancestral thermal sensitivity in the developmental pathways underlying gonadal differentiation? Results from an expression study of a gene involved in early gonadogenesis in GSD (Apalone mutica) and TSD (Chrysemys picta) turtles, support the hypothesis that Wt1 in A. mutica displays such a relic thermal sensitivity. This retention is likely enabled by Sf1, a gene immediately downstream from Wt1 whose expression is independent of temperature in this species. My results constitute the first empirical evidence of a GSD vertebrate exhibiting thermal sensitivity in the expression of a gene regulating gonadogenesis. This novel finding reveals an undocumented source of raw material for future evolutionary change that may exist in other GSD taxa, and one that enhances the evolutionary potential of the gene networks underlying sexual differentiation and contributes to the astonishing ability of sex‐determining mechanisms.     

Phylogeny of sex‐determining mechanisms in squamate reptiles: are sex chromosomes an evolutionary trap?

Squamate reptiles possess two general modes of sex determination: (1) genotypic sex determination (GSD), where the sex of an individual is determined by sex chromosomes, i.e. by sex‐specific differences in genotype; and (2) temperature‐dependent sex determination (TSD), where sex chromosomes are absent and sex is determined by nongenetic factors. After gathering information about sex‐determining mechanisms for more than 400 species, we employed comparative phylogenetic analyses to reconstruct the evolution of sex determination in Squamata. Our results suggest relative uniformity in sex‐determining mechanisms in the majority of the squamate lineages. Well‐documented variability is found only in dragon lizards (Agamidae) and geckos (Gekkota). Polarity of the sex‐determining mechanisms in outgroups identified TSD as the ancestral mode for Squamata. After extensive review of the literature, we concluded that to date there is no known well‐documented transition from GSD to TSD in reptiles, although transitions in the opposite direction are plentiful and well corroborated by cytogenetic evidence. We postulate that the evolution of sex‐determining mechanisms in Squamata was probably restricted to the transitions from ancestral TSD to GSD. In other words, transitions were from the absence of sex chromosomes to the emergence of sex chromosomes, which have never disappeared and constitute an evolutionary trap. This evolutionary trap hypothesis could change the understanding of phylogenetic conservatism of sex‐determining systems in many large clades such as butterflies, snakes, birds, and mammals. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156 , 168–183.     

CLIMATE PREDICTORS OF LATE QUATERNARY EXTINCTIONS

Between 50,000 and 3,000 years before present (BP) 65% of mammal genera weighing over 44 kg went extinct, together with a lower proportion of small mammals. Why species went extinct in such large numbers is hotly debated. One of the arguments proposes that climate changes underlie Late Quaternary extinctions, but global quantitative evidence for this hypothesis is still lacking. We test the potential role of global climate change on the extinction of mammals during the Late Quaternary. Our results suggest that continents with the highest climate footprint values, in other words, with climate changes of greater magnitudes during the Late Quaternary, witnessed more extinctions than continents with lower climate footprint values, with the exception of South America. Our results are consistent across species with different body masses, reinforcing the view that past climate changes contributed to global extinctions. Our model outputs, the climate change footprint dataset, provide a new research venue to test hypotheses about biodiversity dynamics during the Late Quaternary from the genetic to the species richness level.     

Sex determination and optimal development in the Moorish gecko,Tarentola mauritanica

Under temperature sex determination (TSD), sex is determined by temperature during embryonic development. Depending on ecological and physiological traits and plasticity, TSD species may face demographic collapse due to climate change. In this context, asymmetry in bilateral organisms can be used as a proxy for developmental instability and, therefore, deviations from optimal incubation conditions. Using Tarentola mauritanica gecko as a model, this study aimed first to confirm TSD, its pattern and pivotal temperature, and second to assess the local adaptation of TSD and variation of asymmetry patterns across four populations under different thermal regimes. Eggs were incubated at different temperatures, and hatchlings were sexed and measured. The number of lamellae was counted in adults and hatchlings. Results were compatible with a TSD pattern with males generated at low and females at high incubation temperatures. Estimated pivotal temperature coincided with the temperature producing lower embryonic mortality, evidencing selection towards balanced sex ratios. The temperature of oviposition was conservatively selected by gravid females. Asymmetry patterns found were likely related to nest temperature fluctuations. Overall, the rigidity of TSD may compromise reproductive success, and demographic stability in this species in case thermal nest choice becomes constrained by climate change.     

Predicting potential impacts of climate change on freshwater fish in Korea

Climate change is expected to have profound effects on the distribution and phenology of species and the productivity of aquatic ecosystem. In this study, we projected the impacts of climate change on the distributions of 22 endemic fish species in Korea with climatic and geographical variables by using species distribution models (SDMs). Six different SDMs – linear discriminant analysis, generalized linear model, classification and regression trees, random forest, support vector machine, and multivariate adaptive regression splines – were implemented for the prediction, and compared for their prediction capacity. The results showed that the random forest displayed the highest predictive power for the prediction of current species distributions. Therefore, the random forest was used to assess the potential impacts of climate change on the distributions of 22 endemic fish species. The results revealed that five species (Acheilognathus yamatsutae, Sarcocheilichthys variegatus wakiyae, Squalidus japonicus coreanus, Microphysogobio longidorsalis, and Liobagrus andersoni) have a high probability of becoming extinct in their respective habitable sub-watersheds by the 2080s due to climate change. The sensitivity analysis of the model showed that geo-hydrological variables such as stream order and altitude and temperature-related variables such as mean temperature in January and difference between the minimum and maximum temperatures exhibited relatively higher importance in their contributions for the prediction of species occurrence than that other variables. The decline of endemic fish species richness, and their occurrence probability due to climate change, would lead to poleward and upward shifts, as well as extinctions of species. Finally, we believe that our projections are useful for understanding how climate change affects the distribution range of endemic species in Korea, while also providing the necessary information to develop preservation and conservation strategies for maintaining endemic fish.