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Mammals, birds, all snakes and most lizards, amphibians, and some gonochoristic (remaining as the same sex throughout the life) fish use specific sex-determining chromosomes or genes (genetic sex determination (GSD)). Some reptiles, however, including all crocodilians studied to date, many turtle and tortoise species, and some lizards, use environmental or temperature-dependent sex determination (TSD)). Global temperature change can skew the sex ratio of TSD animals and might have played a significant role in the demise of long-extinct species, notably the dinosaurs, particularly if the temperature change resulted in a preponderance of males. Current global warming also represents a risk for extant TSD species. TSD is the dominant mechanism for sex determination in most reptilian species (apart from most speciose lineage - Squamata, lizards).
Patterns of TSD
Sex ratios of TSD reptiles exhibit three general patterns of response to temperature:
- Males at low temperature, females at high (MF or Type 1A) characteristic to turtles;
- Females at low, males at high (FM or Type 1B) occurring in some lizards;
- Females at low and high with males (or both sexes) at intermediate temperatures (FMF or Type II) present in crocodilians and some lizards.
The relationship between sex ratio and egg incubation at constant temperature in TSD species is characterized by two parameters:
- Pivotal temperature (P) - the constant temperature at which both sexes are produced in equal proportions (1:1).
- Transitional range of temperature (TRT) - the range of constant temperatures that yields both sexes in variable proportions. For example, in turtles with MF TSD, TRTs range between 0.7 °C to at least 8.5 °C.
TSD patterns and their associated P and TRT values are inferred from incubation of eggs at constant temperatures in laboratory. Under field conditions, where temperature fluctuates within the nest during the whole incubation period, P is sometimes used to estimate the sex ratio of nests in the wild. The value of P is an index of the temperature where there is a switch from a majority of one sex produced to the other. An indirect method of estimating sex ratios in natural nests from P is thus based on the proportion of the temperature sensitive period of incubation during which the temperature is above P.
The response of sex determination to intermediate temperatures of incubation is variable between embryos. The variability is attributed to genetic and epigenetic effects. For genetic variations to be expressed the incubation temperatures should be within transitional range, because extremely high or low temperatures will override any genetic component or worse - kill all embryos.
Risk factors (not exhaustive list)
Narrow transitional range of temperature (TRT)Species with a wider TRT should be more likely to evolve in response to new thermal conditions and are at lower risk of extinction because greater proportions of mixed sex nests are produced. Also, more heritable genetic variations can be expressed at intermediate temperatures giving the species more chances to evolve in response to climate change.
Lower transitional range of temperature (TRT)For populations with lower TRT values, the consequences to climate change could be dramatic if thermal conditions that allow differentiation of both sexes are no longer available for incubating eggs.
FM TSD patternMale biases are more directly threatening than female biases. Male biases would be predicted for species with FM TSD (tuatara and some squamates), whereas female biases are more likely for species with the MF pattern (most turtles).
Long generation lengthThe generation lengths of some reptiles are among the longest known for any vertebrates and will be a critical limiting factor in determining the rates of adaptation to warmer climates. There is a strong correlation between extinction risk and generation lengths in vertebrates, with species with relatively long generation times being the least likely to persist at small population sizes. Species with short generation lengths (GLs) include agamid lizards (e.g. Ctenophorus pictus – GL = 1 year), whilst the longest generation times include those recorded for turtles (GL = 23–35 years) and tuatara (GL = >40 years)].
Equatorial habitatReptiles that occur at or near the equator may be particularly vulnerable to climate change because they are adapted to a relatively stable climate with markedly smaller daily and seasonal temperature fluctuations than their counterparts at higher latitudes. Consequently, such climate-induced stabilizing selection should deplete adaptive genetic variation compared to fluctuating selection experienced by reptile populations that occur toward the poles. Hence, relative to equatorial species, temperate-zone reptiles are more likely to have retained genetic variation that will allow them to respond adaptively to climate change.
Low dispersal abilityReptiles with TSD have varying levels of vagility, ranging from marine turtles that cross major oceans and that produce hatchlings that disperse on ocean currents, to freshwater turtles and crocodilians that undergo seasonal migrations across wetland and river systems, to terrestrial tortoises and tuatara that have small home ranges and may move less than 1 km in their lifetime. Animal species with low vagility (and their plant counterparts that have limited seed dispersal) may be most likely to require 'assisted migration' (see below) to relocate to more suitable habitats.
Small population sizeThe most dramatic consequence of sex ratio bias is population extinction, but the adaptive potential of small populations may further be eroded by a consistent bias towards one sex. Such populations will lose heterozygosity at a greater rate, and this effect is exacerbated if the skew is more extreme. Loss of heterozygosity is problematic if behavioral or physiological traits associated with TSD in a population are heritable, rather than solely environmentally determined.
Adaptation in phenology
Four traits are likely to serve as primary targets of sex ratio selection in species with TSD:
- pivotal temperature (P);
- transitional range of temperature (TRT);
- nest-site choice;
- nesting phenology.
The first two traits embody the intercept and slope of the temperature- sex ratio reaction norm for developing embryos, whereas the latter two traits encompass spatial and temporal targeting of the embryonic thermal environment. For only one of these traits – nesting phenology – are there extensive data on the response of the trait to warmer climates.
Longer-term studies are revealing that a variety of reptiles with TSD are nesting earlier in warmer years, with the most dramatic shift reported in slider turtles (Trachemys scripta) that have shifted the onset of the nesting season forward by 27 days over 13 years of monitoring, during which period the mean annual temperature has warmed by about 2 °C. This forward shift in the average egg-laying date has also been widely observed in invertebrates, amphibians, and birds. The outcome in terms of offspring sex for reptiles with TSD is largely unknown, and will depend on whether the thermosensitive period (TSP) for sex determination falls in a cooler or warmer portion of the year relative to typical nesting dates. In tuatara, where the TSP occurs between 30–35% of embryonic development, mechanistic models suggest that the effect of earlier nesting in response to a climate 3–4 °C warmer than at present would need to be dramatic (e.g. a forward shift of approximately 90 days by 2085) in order to avoid male-biased sex ratios. Changes in nesting phenology to offset the impact of climate change on offspring sex ratio are similarly predicted to be ineffective in painted turtles (Chrysemys picta).
After Miller D, Summers J, Silber S. Environmental versus genetic sex determination: a possible factor in dinosaur extinction? Fertil Steril. 2004 Apr;81(4):954-64.
In the unfortunate absence of living specimens, we cannot know whether dinosaurs used TSD. Dinosaurs and crocodiles are members of the Archosauria, a major group of diapsids that appeared in the Early Triassic period (~245 MYA). Modern birds were probably derived from avian archosaurs that first appeared during the Jurassic period and expanded their range in the Cretaceous period.
Crocodilians (TSD) and avian (GSD) are only Aurchosaurian taxa that have persisted to this day. Assuming a post-Cretaceous-Tertiary boundary (K-T) global environmental catastrophe, crocodilians but not dinosaurs must have been able to adapt successfully to the changing environment. Perhaps physical and biological constraints did not favor adaptable modes of TSD in dinosaurs.
Ectothermy allows species "to choose" between TSD and GSD. In nature, there are examples of animals that occasionally use both (for example, tilapia, Oreochromis niloticus). Why, did many reptilian species evolve to use GSD exclusively? Most likely because GSD modes are immune to the climate changes as well as random weather fluctuations that challenge animals with TSD and strong selection favors the adoption of GSD in environments in which change in temperature becomes a threat to species survival.
However, there must have been significant adaptive advantages for animals with TSD in much warmer Jurassic climate because higher incubation temperatures (like, for example, higher than physiological limits for endotherms' body temperatures) would allow faster growth rates, larger adult size and enhanced fecundity. Thus, TSD might have given animals the flexibility to exploit niches that might not have otherwise been available to them, and there is no reason to believe that dinosaurs would not also have benefited although even the best known fossil evidence is unable to shed light on details of dinosaurs' sex determination.
Assuming that dinosaurs used TSD, the question is how much skew could species endure and for how long before its extinction was inevitable? Mathematical approach that not only considers population growth rates but also includes approximate breeding dynamics (at minimum, male:female ratio, polygamy, and birth and death rates) must be used to answer this question. According to this model, assuming that the sex ratio skewed from 50:50 (male/female) to 91:9 after the disaster and that, on average, each male mated with four females in each reproductive cycle, populations would still robustly recover after an initial decline, provided the skew was lost within 50 subsequent cycles. However, populations would inexorably decline toward extinction if the skew was to take longer than 50 cycles to abrogate. Fine-tuning the permitted recovery period from an initial modest skew of 60:40 demonstrates that there is the fine dividing line between likely recovery of the population or its inevitable demise. The model does not take into account predator/prey relationship, decreased survival rates under unfavorable conditions, conspecific aggression, epidemics, etc.
It is clear that avian archosaurs were in good position to survive the K-T event, 65 MYA ago, because they had evolved a GSD system. But why did TSD animals like crocodilians and turtles survive? One possibility is that these animals live at the intersection of aquatic and terrestrial environments, in estuarine waters and river beds, which might have afforded some protection against the more extreme effects of environmental change, hence giving them more time to adapt
Contemporary climate change has already exerted an impact, and will continue to threaten the viability of many species, largely through interactions with other deleterious processes such as habitat fragmentation and disease. Data available on the factors that threaten individual species of reptiles are scarce relative to data that are available for mammals and birds, yet a recent assessment by the International Union for Conservation of Nature (IUCN) concludes that 22% of the world's reptile species are at risk of extinction – a proportion similar to the 25% for mammals and birds. Reptiles with TSD may serve as 'canaries in the coalmine' for the biological impacts of rapid climate change, because few threshold traits are as fundamental to population viability as those that determine sex.
- "Climate+TSD" (free articles from PubMed Central)
- Miller D, Summers J, Silber S. Environmental versus genetic sex determination: a possible factor in dinosaur extinction? Fertil Steril. 2004 Apr;81(4):954-64.
- Mitchell NJ, Kearney MR, Nelson NJ, Porter WP. Predicting the fate of a living fossil: how will global warming affect sex determination and hatching phenology in tuatara? Proc Biol Sci. 2008 October 7; 275(1648): 2185–2193.
- Huey RB, Janzen FJ. Climate warming and environmental sex determination in tuatara: the Last of the Sphenodontians? Proc Biol Sci. 2008 October 7; 275(1648): 2181–2183.
- Ospina-Alvarez N, Piferrer F. Temperature-Dependent Sex Determination in Fish Revisited: Prevalence, a Single Sex Ratio Response Pattern, and Possible Effects of Climate Change.
PLoS ONE. 2008; 3(7): e2837.
They are defined according to the sex ratio produced as a function of temperature during the thermosensitive period.
A, Pattern 1, low temperatures produce female-biased sex ratios and high temperatures produce male-biased sex ratios.
B, Pattern 2, low temperatures produce male-biased sex ratios and high temperatures produce female-biased sex ratios.
C, Pattern 3, male-biased sex ratios are produced at low and high temperatures, while balanced sex ratios are produced at intermediate temperatures. In some cases, the response may be partial (dashed line in A).
The present study demonstrates that fish species with TSD only exhibit pattern 1.
- Neuwald JL, Valenzuela N. The lesser known challenge of climate change: thermal variance and sex-reversal in vertebrates with temperature-dependent sex determination.
PLoS One. 2011 Mar 23;6(3):e18117.
Observed effects of increased mean temperature and increased thermal variance on life history parameters of the TSDIa turtle, Chrysemys picta, and implications in the context of climate change predictions. Effects are divided into three thermal ranges: optimal temperatures (OTR), colder temperatures below the OTR, and warmer temperatures above the OTR. Inner cells correspond to neutral effects (gray), beneficial effects (green), and detrimental effects (pink) on developmental rate, embryonic survival, and sex ratio, as described in the text. Listed effects correspond to those of increased mean temperature alone under low or no variance scenarios, and to those of increased thermal variance when compared to mean temperature effects.
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