Demographic effects of temperature‐dependent sex determination: will tuatara survive global warming?

Global climate change is of particular concern for small and isolated populations of reptiles with temperature-dependent sex determination because low genetic variation can limit adaptive response in pivotal temperatures, leading to skewed sex ratios. We explore the demographic consequences of skewed sex ratios on the viability of a tuatara population characterized by low genetic diversity. We studied the rare species of tuatara ( Sphenodon guntheri ) on the 4 ha North Brother Island in New Zealand over two nesting seasons and captured 477 individuals, with a 60% male bias in the adult population. Females first breed at 15 years and have extremely low rates of gravidity, producing clutches of three to eight eggs every 9 years. Simulations of the population using population viability analysis showed that the current population is expected to persist for at least 2000 years at hatchling sex ratios of up to 75% male, but populations with 85% male hatchlings are expected to become extinct within approximately 300 years (some eight generations). Incorporation of inbreeding depression increased the probability of extinction under male biased sex ratios, with no simulated populations surviving at hatchling sex ratios >75% male. Because recent models have predicted that climate change could lead to the production of all male S. guntheri hatchlings by 2085, we examined whether periodic intervention to produce mixed or female biased sex ratios would allow the population to survive if only males were produced in natural nests. We show that intervention every 2–3 years could buffer the effects of climate change on population sex ratios, but translocation to cooler environs might be more cost-effective. Climate change threatens tuatara populations because neither modified nesting behaviour nor adaptive response of the pivotal temperature can modify hatchling sex ratios fast enough in species with long generation intervals.     

Does flower phenology mirror the slowdown of global warming?

Although recent global warming trends in air temperature are not as pronounced as those observed only one decade ago, global mean temperature is still at a very high level. Does plant phenology – which is believed to be a suitable indicator of climate change – respond in a similar way, that is, does it still mirror recent temperature variations? We explored in detail long-term flowering onset dates of snowdrop, cherry, and lime tree and relevant spring temperatures at three sites in Germany (1901–2012) using the Bayesian multiple change-point approach. We investigated whether mean spring temperature changes were amplified or slowed down in the past decade and how plant phenology responded to the most recent temperature changes. Incorporating records with different end points (i.e., 2002 and 2012), we compared differences in trends and inferred possible differences caused by extrapolating phenological and meteorological data. The new multiple-change point approach is characterized by an enhanced structure and greater flexibility compared to the one change point model. However, the highest model probabilities for phenological (meteorological) records were still obtained for the one change point (linear) model. Marked warming trends in the recent decade were only revealed for mean temperatures of March to May, here better described with one or two change point models. In the majority of cases analyzed, changes in temperatures were well mirrored by phenological changes. However, temperatures in March to May were linked to less strongly advancing onset dates for lime tree flowering during the period 1901-2012, pointing to the likely influence of photoperiodic constraints or unfulfilled chilling requirements. Due to the slowdown of temperature increase, analyses conducted on records ending in 2002 demonstrated distinct differences when compared with records ending in 2012. Extrapolation of trends could therefore (along with the choice of the statistical method) lead to distinctly different results and most recent data should be integrated in order not to over- or underestimate future phenological changes.     

Macroevolutionary patterns in Rhynchocephalia: is the tuatara (Sphenodon punctatus) a living fossil?

The tuatara, Sphenodon punctatus, known from 32 small islands around New Zealand, has often been noted as a classic ‘living fossil’ because of its apparently close resemblance to its Mesozoic forebears and because of a long, low‐diversity history. This designation has been disputed because of the wide diversity of Mesozoic forms and because of derived adaptations in living Sphenodon. We provide a testable definition for ‘living fossils’ based on a slow rate of lineage evolution and a morphology close to the centroid of clade morphospace. We show that through their history since the Triassic, rhynchocephalians had heterogeneous rates of morphological evolution and occupied wide morphospaces during the Triassic and Jurassic, and these then declined in the Cretaceous. In particular, we demonstrate that the extant tuatara underwent unusually slow lineage evolution, and is morphologically conservative, being located near the centre of the morphospace for all Rhynchocephalia.     

Growth and sex ratio of nestlings in two species of crows: how important is hatching asynchrony?

Summary In experimental studies of avian hatching paterns offspring sex has been neglected. This may be a problem if nestling growth and mortality is sex biased, and if this bias is influenced by hatching spread. In a field study of two crow species, the magpie Pica pica and the hooded crow Corvus corone cornix, we manipulated hatching spread. Both species have asynchronous hatching, and adult males are larger than females by 12–14%. The sex ratios obtained from the different experimental groups on day 24 post-hatch (total sample n = 403) did not deviate significantly from unity, nor did the sex ratios obtained among young newly hatched in an incubator (total sample n = 305). Male and female offspring were of similar size at hatching but males were larger on day 24 post-hatch. Males seemed to be more costly to rear than females, judging by the 20% difference in the mean amounts of food found in the gizzards of the young on day 24 post-hatch. Dimorphism in body size did not seem to be influenced by degree of hatching spread. Asynchronous hatching did not seem to be needed to produce high quality offspring of the larger sex (i.e. males), nor did asynchronous hatching help to ensure equal parental investment in male and female progeny. One reason for the latter negative results may be that the size dimorphism of the two crow species studied were relatively small.     

Climate change and temperature-dependent sex determination: can individual plasticity in nesting phenology prevent extreme sex ratios?

Under temperature-dependent sex determination (TSD), temperatures experienced by embryos during development determine the sex of the offspring. Consequently, populations of organisms with TSD have the potential to be strongly impacted by climatic warming that could bias offspring sex ratio, a fundamental demographic parameter involved in population dynamics. Moreover, many taxa with TSD are imperiled, so research on this phenomenon, particularly long-term field study, has assumed great urgency. Recently, turtles with TSD have joined the diverse list of taxa that have demonstrated population-level changes in breeding phenology in response to recent climate change. This raises the possibility that any adverse impacts of climate change on populations may be alleviated by individual plasticity in nesting phenology. Here, we examine data from a long-term study on a population of painted turtles (Chrysemys picta) to determine whether changes in phenology are due to individual plasticity and whether individual plasticity in the timing of nesting has the capacity to offset the sex ratio effects of a rise in climatic temperature. We find that individual females show plasticity in the date of first nesting each year, and that this plasticity depends on the climate from the previous winter. First nesting date is not repeatable within individuals, suggesting that it would not respond to selection. Sex ratios of hatchlings within a nest declined nonsignificantly over the nesting season. However, small increases in summer temperature had a much stronger effect on nest sex ratios than did laying nests earlier in the season. For this and other reasons, it seems unlikely that individual plasticity in the timing of nesting will offset the effects of climate change on sex ratios in this population, and we hypothesize that this conclusion applies to other populations with TSD.     

The effect of temperature on sex ratio in the isopod Porcellionides pruinosus: Environmental sex determination or a by-product of cytoplasmic sex determination?

The sex ratios of the progenies of woodlice Porcellionides pruinosus (Crustacea, Isopoda) raised at different temperatures were studied. Females from three French populations sampled in the wild produced highly female-biased broods at 20°C and male-biased broods above 30°C. The effect of high temperature was not due to selective mortality of females. Sex determination was thus sensitive to temperature in P. pruinosus. We also found an interpopulation variability of sex ratio thermosensitivity and a weak inheritance of male-biased sex ratios at high temperatures. Samples taken from a wild population throughout the year showed that while the thermal conditions required for changes in the sex ratio occurred, there was no significant variation in the sex ratio. On the other hand, almost all the females and many males in the four populations studied harboured intracytoplasmic bacteria. These maternally inherited symbionts belong to the genus Wolbachia and are known to possess a feminizing effect. While in other arthropods Wolbachia are destroyed at high temperatures, the symbionts of P. pruinosus were detected by a PCR procedure whatever the rearing temperatures. In light of these results, we propose that the thermosensitivity of sex determination in P. pruinosus could reflect the removal of the cytoplasmic effect on sex determination rather than environmental sex determination sensu stricto. The reduction in the amount of bacteria (but not their entire elimination), or the inhibition of bacterial metabolism, may be responsible for sex ratio variations relating to temperature. The incomplete inheritance of male-biased sex ratios at high temperatures might reflect a selection of thermo-tolerant bacterial strains.     

Germ-line determination in Caenorhabditis and Ascaris: will a helicase begin to unravel the mystery?

How cell lineages are established during development in higher eukaryotes is being addressed by geneticists and by developmental and molecular biologists. In Drosophila melanogaster, a gene corresponding to a germ-line-specific RNA helicase, vasa, has been shown to be a component o f the posteriorly localized germ granules o f the developing embryo. A putative RNA helicase, glh-I r which appears germ-line specific in its expression, has recently been reported from the free-living nematode Caenorhabditis elegans. Parasitologists studying the nematode Ascaris lumbricoides var. suum have found it to be a useful complement to Caenorhabditis. Deborah Roussell, Michael Gruidl and Karen Bennett predict that Ascaris will be valuable in determining the role played by germ-line helicases in development.     

Temperature-dependent sex determination and global change: are some species at greater risk?

In species with temperature-dependent sex determination (TSD), global climate change may result in a strong sex ratio bias that could lead to extinction. The relationship between sex ratio and egg incubation at constant temperature in TSD species is characterized by two parameters: the pivotal temperature (P) and the transitional range of temperature that produces both sexes (TRT). Here, we show that the proportion of nests producing both sexes is positively correlated to the width of the TRT by a correlative approach from sex ratio data collected in the literature and by simulations of TSD using a mechanistic model. From our analyses, we predict that species with a larger TRT should be more likely to evolve in response to new thermal conditions, thus putting them at lower risk to global change.     

Does irrigation affect leaf phenology in deciduous and evergreen trees of the savannas of northern Australia?

Abstract Soil moisture was augmented experimentally during two successive dry seasons and the intervening wet season in a humid tropical savanna in Darwin, northern Australia. Leaf phenology was monitored in four common tree species Termmalia ferdinandiana and Planchonia careya (both deciduous species), and Eucalyptus miniata and Eucalyptus tetrodonta (both evergreen species). Irrigation produced consistently significant effects in only T. ferdinandiana. In this species leaf-flush was significantly earlier, canopy decline and leaf-fall were significantly later and the attainment of full canopy was earlier in irrigated compared with non-irrigated trees. Litterfall, and the seasonal patterns of contraction and expansion of stems (a measure of stem water status or storage) were not significantly affected by irrigation in any species. Leaf longevity in the deciduous species was 6–8 months; some eucalypt leaves lived for approximately 1 year, but none lived longer than 18 months. Irrigation had relatively little effect on leaf longevity. While variation in soil moisture is a potentially important cue to both leaf-fall and leaf-flush, stem water status and climatic factors such as vapour pressure deficit may also be important climatic cues to phenological behaviour.     

Cellular calcium and redox regulation: the mediator of vertebrate environmental sex determination?

Many reptiles and some fish determine offspring sex by environmental cues such as incubation temperature. The mechanism by which environmental signals are captured and transduced into specific sexual phenotypes has remained unexplained for over 50 years. Indeed, environmental sex determination (ESD) has been viewed as an intractable problem because sex determination is influenced by a myriad of genes that may be subject to environmental influence. Recent demonstrations of ancient, conserved epigenetic processes in the regulatory response to environmental cues suggest that the mechanisms of ESD have a previously unsuspected level of commonality, but the proximal sensor of temperature that ultimately gives rise to one sexual phenotype or the other remains unidentified. Here, we propose that in ESD species, environmental cues are sensed by the cell through highly conserved ancestral elements of calcium and redox (CaRe) status, then transduced to activate ubiquitous signal transduction pathways, or influence epigenetic processes, ultimately to drive the differential expression of sex genes. The early evolutionary origins of CaRe regulation, and its essential role in eukaryotic cell function, gives CaRe a propensity to be independently recruited for diverse roles as a ‘cellular sensor’ of environmental conditions. Our synthesis provides the first cohesive mechanistic model connecting environmental signals and sex determination pathways in vertebrates, providing direction and a framework for developing targeted experimentation.     

Is intersexuality a cost of environmental sex determination in Gammarus duebeni?

Three possible causes of intersexuality in Gammarus duebeni , a crustacean with environmental sex determination, were investigated. Intersexuality appears to be a cost of the flexible sex-determining mechanism of this species: the occurrence of intersexes is influenced by photoperiod, which also cues sex determination. Intersexuality is heritable: intersex mothers produce more intersex offspring than do true females. Parasitism by a feminizing microsporidian is ruled out as a significant cause of intersexuality.     

Biological consequences of global warming: is the signal already apparent?

Increasing greenhouse gas concentrations are expected to have significant impacts on the world's climate on a timescale of decades to centuries. Evidence from long-term monitoring studies is now accumulating and suggests that the climate of the past few decades is anomalous compared with past climate variation, and that recent climatic and atmospheric trends are already affecting species physiology, distribution and phenology.