Benoit Heulin

Erosion of lizard diversity by climate change and altered thermal niches

Demise of the Lizards Despite pessimistic forecasts from recent studies examining the effects of global climate change on species, and observed extinctions in local geographic areas, there is little evidence so far of global-scale extinctions. Sinervo et al. (p. 894; see the Perspective by Huey et al.) find that extinctions resulting from climate change are currently reducing global lizard diversity. Climate records during the past century were synthesized with detailed surveys of Mexican species at 200 sites over the past 30 years. Temperature change has been so rapid in this region that rates of adaptation have not kept pace with climate change. The models were then extended to all families of lizards at >1000 sites across the globe, and suggest that climate change-induced extinctions are currently affecting worldwide lizard assemblages. A historical record of lizard populations in Mexico is used to parameterize models that predict global effects of climate change. It is predicted that climate change will cause species extinctions and distributional shifts in coming decades, but data to validate these predictions are relatively scarce. Here, we compare recent and historical surveys for 48 Mexican lizard species at 200 sites. Since 1975, 12% of local populations have gone extinct. We verified physiological models of extinction risk with observed local extinctions and extended projections worldwide. Since 1975, we estimate that 4% of local populations have gone extinct worldwide, but by 2080 local extinctions are projected to reach 39% worldwide, and species extinctions may reach 20%. Global extinction projections were validated with local extinctions observed from 1975 to 2009 for regional biotas on four other continents, suggesting that lizards have already crossed a threshold for extinctions caused by climate change.

Models of density-dependent genic selection and a new rock-paper-scissors social system.

We describe new ESS models of density regulation driven by genic selection to explain the cyclical dynamics of a social system that exhibits a rock‐paper‐scissors (RPS) set of three alternative strategies. We tracked changes in morph frequency and fitness of Lacerta vivipara and found conspicuous RPS cycles. Morphs of Uta and Lacerta exhibited parallel survival‐performance trade‐offs. Frequency cycles in both species of lizards are driven by genic selection. In Lacerta, frequency of each allele in adult cohorts had significant impacts on juvenile recruitment, similar to mutualistic, altruistic, and antagonistic relations of RPS alleles in Uta. We constructed evolutionarily stable strategy (ESS) models in which adults impact juvenile recruitment as a function of self versus nonself color recognition. ESS models suggest that the rapid 4‐year RPS cycles exhibited by Lacerta are not possible unless three factors are present: behaviors evolve that discriminate self versus nonself morphs at higher rates than random, self‐ versus non‐self‐recognition contributes to density regulation, and context‐dependent mate choice evolves in females, which choose sire genotypes to enhance progeny survival. We suggest genic selection coupled to density regulation is widespread and thus fundamental to theories of social system evolution as well as theories of population regulation in diverse animal taxa.

Multilocus phylogeography of the common lizard Zootoca vivipara at the Ibero-Pyrenean suture zone reveals lowland barriers and high-elevation introgression

BackgroundThe geographic distribution of evolutionary lineages and the patterns of gene flow upon secondary contact provide insight into the process of divergence and speciation. We explore the evolutionary history of the common lizard Zootoca vivipara (= Lacerta vivipara) in the Iberian Peninsula and test the role of the Pyrenees and the Cantabrian Mountains in restricting gene flow and driving lineage isolation and divergence. We also assess patterns of introgression among lineages upon secondary contact, and test for the role of high-elevation trans-mountain colonisations in explaining spatial patterns of genetic diversity. We use mtDNA sequence data and genome-wide AFLP loci to reconstruct phylogenetic relationships among lineages, and measure genetic structure.ResultsThe main genetic split in mtDNA corresponds generally to the French and Spanish sides of the Pyrenees as previously reported, in contrast to genome-wide AFLP data, which show a major division between NW Spain and the rest. Both types of markers support the existence of four distinct and geographically congruent genetic groups, which are consistent with major topographic barriers. Both datasets reveal the presence of three independent contact zones between lineages in the Pyrenean region, one in the Basque lowlands, one in the low-elevation mountains of the western Pyrenees, and one in the French side of the central Pyrenees. The latter shows genetic evidence of a recent, high-altitude trans-Pyrenean incursion from Spain into France.ConclusionsThe distribution and age of major lineages is consistent with a Pleistocene origin and a role for both the Pyrenees and the Cantabrian Mountains in driving isolation and differentiation of Z. vivipara lineages at large geographic scales. However, mountain ranges are not always effective barriers to dispersal, and have not prevented a recent high-elevation trans-Pyrenean incursion that has led to asymmetrical introgression among divergent lineages. Cytonuclear discordance in patterns of genetic structure and introgression at contact zones suggests selection may be involved at various scales. Suture zones are important areas for the study of lineage formation and speciation, and our results show that biogeographic barriers can yield markedly different phylogeographic patterns in different vertebrate and invertebrate taxa.

Calcium provision to oviparous and viviparous embryos of the reproductively bimodal lizard Lacerta (Zootoca) vivipara.

SUMMARY Embryos of oviparous squamate reptiles typically obtain calcium from both yolk and eggshell but differ from other oviparous amniotes (turtles, birds and crocodilians) because they are heavily dependent on calcium-rich yolk. Eggs of viviparous squamates lack calcareous eggshells, and embryos receive calcium solely from yolk or from both yolk and placenta. The pattern of calcium mobilization by amniote embryos has been predicted to influence the evolution of viviparity if embryos are dependent on calcium from the eggshell and calcium placentotrophy evolves subsequent to viviparity. We studied the pattern of maternal provision and embryonic utilization of calcium of an oviparous and a viviparous population of the reproductively bimodal lizard Lacerta vivipara to test the hypotheses: (1) oviparous embryos are not dependent on eggshell calcium and (2) calcium content of viviparous hatchlings does not differ from oviparous hatchlings. Our findings do not support either of these hypotheses because oviparous females oviposited eggs with heavily calcified shells and calcium-poor yolk, and embryonic mobilization of shell calcium was greater than for other oviparous squamates. The calcium content of yolk from viviparous females did not differ from oviparous yolk, but viviparous eggs lacked calcareous eggshells. Uterine secretion by viviparous females compensated for the low calcium content of yolk, and placental calcium transfer was among the highest recorded for squamates. The pattern of calcium provision in these two populations suggests that dependence on uterine calcium, either stored temporarily in an eggshell or transferred directly across a placenta, did not constrain the evolution of reproductive mode in this lineage.

Cytokines in the oviparity/viviparity transition: evidence of the interleukin‐1 system in a species with reproductive bimodality, the lizard Lacerta vivipara

Summary Placental viviparity is a reproductive strategy usually attributed to mammals. However, it is also present in other vertebrate species, e.g. in Squamate reptiles. Although the immunological mechanisms that allow the survival of the semi‐allogenic embryo in maternal tissues are still largely unknown, cytokines seem to play an important role in mammalian reproduction. Previous studies in our laboratory showed that interleukin‐1 (IL‐1), a cytokine associated with implantation in mice, is also expressed at the materno‐fetal interface of placental viviparous Squamates. In this study, we used the model of Lacerta vivipara, which exhibits reproductive bimodality, that is, the coexistence of oviparous and viviparous populations. By means of immunohistochemistry and anti‐human antibodies, we showed that uterine tissues of L. vivipara (seven oviparous and six viviparous animals) expressed the two IL‐1 isoforms, IL‐1α and IL‐1β, and the type I IL‐1 receptor (IL‐1R tI) both at the pre‐ovulatory stage and during gestation, with no significant difference between oviparous and viviparous females. In L. vivipara, as in most oviparous Squamates, an important phase of embryonic development takes place in the mothers oviduct, before egg‐laying. Moreover, although thinner than in oviparous females, an eggshell membrane persists throughout gestation in viviparous females also, which develop a very simple type of placenta. The data suggest that immunological mechanisms that allow the survival of the semi‐allogenic embryo in maternal tissues are independent of the timing or intimacy of contact between maternal and fetal tissues.

Influence of reproductive mode on metabolic costs of reproduction: insight from the bimodal lizard Zootoca vivipara

Examination of the selective forces behind the transition from oviparity to viviparity in vertebrates must include an understanding of the relative energy costs of the two reproductive modes. However, interspecific comparisons of reproductive mode are confounded by numerous other inherent differences among the species. Therefore, we compared oxygen consumption, as a reflection of energy costs, during reproduction in oviparous and viviparous females of the reproductively bimodal lizard Zootoca vivipara (Jaquin 1787). Female oxygen consumption progressively increased over the course of reproduction, peaking just prior to parition when it was 46% (oviparous form) and 82% (viviparous form) higher than it was at the pre-reproductive stage. Total increase in oxygen consumption (TIOC) during the pre-ovulation period was not different between the reproductive modes. Conversely, post-ovulation TIOC was more than three times higher in viviparous females, reflecting a dramatic increase in embryonic metabolism as well as maternal metabolic costs of pregnancy (MCP). MCP accounted for 22% of total metabolism in viviparous females, whereas it was negligible in oviparous females. Our results demonstrate that egg retention through the first third of development, as is typical of most oviparous squamates, entails minimal maternal energy demand, while extending retention imposes much greater metabolic constraints. Selection for transition from oviparity to viviparity must therefore provide benefits that outweigh not only the added burden associated with prolonged embryonic retention, but also the substantial additional energy costs that are incurred.

Mitochondrial and Nuclear DNA Survey of Zootoca vivipara across the Eastern Italian Alps: Evolutionary Relationships, Historical Demography and Conservation Implications

The European common lizard Zootoca vivipara exhibits reproductive bimodality, with populations being either viviparous or oviparous. In the central-eastern Italian Alps oviparous populations (Z. v. carniolica) and viviparous populations (Z. v. vivipara) partly overlap geographically. Studying the evolutionary relationship between these taxa presents an interesting opportunity to gain insight into the evolution of this trait. We aim to: i) test whether Z. v. carniolica, which is endangered, constitutes an ESU (Evolutionary Significant Unity); ii) infer mtDNA divergence time between the Z. v. carniolica clade and all the other Z. vivipara subspecies with the aid of an external calibration point; and iii) describe the phylogeographical and demographic scenarios in the area. To do so we sequenced about 200 individuals for mitochondrial variation; 64 of them were also analysed for three nuclear genes. Furthermore, we analysed the same nuclear markers in 17 individuals from the other oviparous subspecies Z. v. louislantzi and 11 individuals of Z. v. vivipara from widespread geographical origins. The mtDNA and nDNA loci that we examined supported the monophyly of Z. v. carniolica. The mtDNA-based estimate of divergence time between Z. v. carniolica and all the other subspecies indicated a separation at 4.5 Mya (95% CI 6.1–2.6), with about 5% of sequence divergence. Considering that Z. v. carniolica harbours higher genetic diversity, while Z. v. vivipara from central-eastern Alps shows a signature of recent population and spatial expansion, we argue that Z. v. carniolica represents a distinct evolutionary unit, with a presumably long-term evolutionary history of separation. Z. v. carniolica populations, occurring at higher latitudes and altitudes than insofar supposed, live in peat bogs, a seriously threatened habitat: taking into account also its evolutionary distinctness, specific conservation measures should be considered.

Developmental expression of calcium transport proteins in extraembryonic membranes of oviparous and viviparous Zootoca vivipara (Lacertilia, Lacertidae)

SUMMARY The eggshell of oviparous lizards is a significant source of calcium for embryos, whereas the eggshell of viviparous lizards, when present, contains little calcium. In view of the potential cost to embryonic nutrition occasioned by the loss of eggshell calcium, the large number of independent origins of viviparity among lizards is surprising. Concomitant evolution of viviparity and calcium placentotrophy would ameliorate the loss of eggshell calcium, but a mechanism linking these events has yet to be discovered. Zootoca vivipara, a lizard with geographic variation in its mode of parity, is an excellent model for studying mechanisms of calcium transport to oviparous and viviparous embryos because each is highly dependent on calcium secreted by the uterus (eggshell or placenta) and ontogenetic patterns of embryonic calcium mobilization are similar. We compared developmental expression of the calcium transport protein calbindin-D28K in yolk splanchnopleure and chorioallantoic membranes of oviparous and viviparous embryos to test the hypothesis that the mechanism of calcium transport does not differ between modes of parity. We found that the ontogenetic pattern of protein expression is similar between reproductive modes and is correlated with calcium uptake from yolk and either eggshell or placenta. Calbindin-D28K is localized in the chorionic epithelium of embryos of both reproductive modes. These findings suggest that the embryonic calcium transport machinery is conserved in the transition between reproductive modes and that an adaptation of oviparous embryos for calcium uptake from eggshells functions similarly to transport calcium directly from uterine secretions.

Temperature Diurne d'Activité des Males et des Femelles de Lacerta vivipara

Mean body temperature (TC) of Lacerta vivpara ranges from 26°8 to 32° at Paimpont (France). There is a highly significant correlation between environmental temperatures (TS) and body temperatures (TC). The mean body temperature of pregnant females is lower than that of males and non-pregnant females. Also, the regression line TC = f(TS) calculated for pregnant females is different from those calculated for males and non-pregnant females. The possible relations between pregnancy and body temperature are discussed.

Further evidence of the existence of oviparous populations of Lacerta (Zootoca) vivipara in the NW of the Balkan Peninsula

The lizard Lacerta (Zootoca) vivipara, which is viviparous in the greatest part of its distribution range, has however some oviparous populations on the southern margin of its range. The present study aimed at determining the reproductive mode and the ATA (aspartate transaminase) enzyme characteristics of four populations in Slovenia and one population in Croatia. The Slovenian females studied here presented an oviparous reproductive mode which strongly resembled those observed in the oviparous populations of south-western France and north-western Spain. Our electrophoresis analyses revealed the existence of two distinct alleles, ATA-150 and ATA-200, in the oviparous populations of Slovenia. These alleles were identical to those observed in the French and Spanish oviparous group and were distinct from the allele ATA-100 characterizing the viviparous populations that we had previously studied. Although we did not study the reproductive mode of Croatian females, the allele ATA-200 observed in one population of Croatia strongly suggested that this population might also be oviparous.