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Dependent Sex Determination at The Downloaded from rsbl.royalsocietypublishing.org on October 27, 2010 Biol. Lett. Indian plate peaked slightly before the K–Pg boundary doi:10.1098/rsbl.2010.0882 [3]. It has been widely suggested that one or both Published online events were responsible for the mass extinction at the Palaeontology K–Pg boundary and that each had profound effects on global climate. The impact vapourized large quantities of evaporite minerals, and the resulting sulphate aerosols Unexpected resilience of probably seeded clouds that reflected solar radiation [4]. The volcanic eruptions, which formed the Deccan Traps species with temperature- of India, released large quantities of CO2 into the atmos- phere and may have initiated global warming [5]. Those dependent sex species that had temperature-dependent sex determi- determination at the nation (TSD) are expected to have been negatively impacted by these climate changes [6,7]. Cretaceous–Palaeogene In TSD, the sex of the embryo is determined by the incubation temperature of the eggs. Incubation at the boundary pivotal temperature(s) yields a 1 : 1 sex ratio, small temp- erature deviations yield an unbalanced sex ratio and 1, 2 Sherman Silber *, Jonathan H. Geisler larger deviations yield single-sex clutches [8]. In genoty- and Minjin Bolortsetseg3 pic sex determination (GSD), a sex-determining gene 1Infertility Center of Saint Louis, St Luke’s Hospital, Saint Louis, activates a downstream cascade of other genes that are MO 63017, USA responsible for testis or ovarian development. The 2New York College of Osteopathic Medicine, Old Westbury, NY 11568, USA specific chromosomes and genes in GSD have evolved 3Institute for the Study of Mongolian Dinosaurs, Ulaanbaatar 14201, independently in numerous lineages, suggesting that it Mongolia has adaptive benefits [7]. Therian mammals employ an *Author for correspondence ([email protected]). XX–XY, male heterogametic system that evolved from It has been suggested that climate change at autosomes when the SRY (testis-determining) gene the Cretaceous–Palaeogene (K–Pg) boundary, emerged on what became the Y chromosome. Exactly initiated by a bolide impact or volcanic when this transformation occurred depends on hom- eruptions, caused species with temperature- ologies of the complicated monotreme XX–XY system dependent sex determination (TSD), including [9]. In contrast, birds employ a female heterogametic dinosaurs, to go extinct because of a skewed sex (ZZ–ZW) system that according to recent experimental ratio towards all males. To test this hypothesis, evidence [10]leadstotesticulardevelopmentwitha the sex-determining mechanisms (SDMs) of Cretaceous tetrapods of the Hell Creek For- double dosage of the Z-linked gene DMRT1. mation (Montana, USA) were inferred using It has been suggested that non-avian dinosaurs had parsimony optimizations of SDMs on a tree, TSD, that temperature change at the K–Pg boundary including Hell Creek species and their extant led to male-dominated populations of non-avian dino- relatives. Although the SDMs of non-avian saurs via TSD and that this imbalance led to their dinosaurs could not be inferred, we were able extinction [6,7]. Although elements of this hypothesis to determine the SDMs of 62 species; 46 had have been criticized (i.e. [11]), there has been no sys- genotypic sex determination (GSD) and 16 had tematic attempt to test whether Cretaceous species TSD. The TSD hypothesis for extinctions per- with TSD were more prone to extinction than their formed poorly, predicting between 32 and 34 per GSD cohorts. Thus, in the present study, we are deter- cent of survivals and extinctions. Most surpris- mining whether Cretaceous species of tetrapods with ingly, of the 16 species with TSD, 14 of them survived into the Early Palaeocene. In contrast, TSD experienced substantially more extinctions than 61 per cent of species with GSD went extinct. those with GSD at the K–Pg boundary. Ideally, several Possible explanations include minimal climate regions would be examined, but unfortunately only the change at the K–Pg, or if climate change did Cretaceous Hell Creek Formation and Early Palaeocene occur, TSD species that survived had egg-laying Tullock Formation display near-continuous non-marine behaviour that prevented the skewing of sex sedimentation across the K–Pg boundary, have an ratios, or had a sex ratio skewed towards female unambiguous K–Pg boundary and have rich and inten- rather than male preponderance. Application of sively studied fossil faunas above and below the molecular clocks may allow the SDMs of non- boundary [12]. avian dinosaurs to be inferred, which would be an important test of the pattern discovered here. Keywords: Cretaceous; temperature-dependent 2. MATERIAL AND METHODS sex determination; extinction Survivorship at the K–Pg boundary was based on table 5.1 of Archi- bald [12], which was compiled from the Hell Creek and Tullock formations of Garfield and McCone Counties, Montana, USA. Minor modifications were made to this table to incorporate studies pub- lished since 1996 (see the electronic supplementary material). 1. INTRODUCTION Explanatory power of the TSD hypothesis is determined by counting Geological evidence indicates that a large bolide hit the number of taxa whose extinction or survival is correctly predicted. the Yucatan Peninsula at the Cretaceous–Palaeogene Taxa that have TSD are predicted to have gone extinct, whereas taxa that have GSD are predicted to have survived. The statistical signifi- (K–Pg) boundary (ca 65.5 Ma) [1,2], whereas other evi- cance of differences in extinction frequencies between species with dence indicates that massive volcanic eruptions on the TSD and those with GSD was determined using Fisher’s exact test of independence [13]inthecomputerapplicationSPSS. Electronic supplementary material is available at http://dx.doi.org/ To infer the SDMs of Hell Creek tetrapods, three character states 10.1098/rsbl.2010.0882 or via http://rsbl.royalsocietypublishing.org. for SDM (XX/XY, ZZ/ZW and TSD) were mapped onto a Received 23 September 2010 Accepted 7 October 2010 This journal is q 2010 The Royal Society Downloaded from rsbl.royalsocietypublishing.org on October 27, 2010 2 S. Silber et al. Effect of K–Pg event on species with TSD phylogeny including extant taxa and Hell Creek species in MAC- Plethodontidae CLADE v. 4.08 [14]. Most parsimonious reconstructions were 2–7 considered for each internal branch, and SDMs were treated as an Ambystomatidae unordered, multistate character. In the absence of total evidence, Salamandridae comprehensive phylogenies that include Hell Creek and extant taxa, SDMs were reconstructed on a well-supported molecular tree Proteidae of tetrapods, with fossil taxa placed next to their closest extant rela- 8 Sirenidae tives, as determined by morphological studies (see the electronic supplementary material). For extant taxa, we used modified versions Leiopelmatidae of the SDM dataset and phylogeny employed by Organ & Janes [15] Pipidae (see the electronic supplementary material). 1 1 Bombinatoridae 1 Discoglossidae 3. RESULTS 1 Pelodytidae The TSD hypothesis was originally developed to 1 explain the extinction of non-avian dinosaurs, but Ranidae 1 unfortunately the SDM of non-avian dinosaurs Hylidae 1 remains speculative because birds, their closest extant Bufonidae relatives [16], have GSD whereas crocodylians, their Leptodactylidae next closest relatives [17], have TSD [6]. The GSD of extant birds evolved somewhere on the branch lead- Ornithorhynchus ing from their common ancestor with crocodylians, so 18–28 Marsupialia 29–35 that it is equally parsimonious to infer that all non- 9– Placentalia avian dinosaurs and basal avialans like Anchiornis and 17 Chelidae Archaeoptetyx had TSD or that all dinosaurs, including Podocnemididae extinct birds, had GSD (figure 1). For the 68 non-dinosaur tetrapods of the Hell Creek Pelomedusidae Formation, SDMs can be inferred in 62 of them Carettochelyidae 44 36 45 (figure 1). GSD is inferred to have occurred in 46 of 47 Trionychidae 46 these species, including allmammals,amphibiansand Emydidae lizards; and TSD is inferred to have occurred in 16 of 37– Testudinidae these species, 11 turtles and all crocodylians. The TSD 41 Chelonidae hypothesis is a very poor predictor of extinction (table 1); of the 32 extinctions and 30 survivals of the Dermochelyidae K–Pg event in eastern Montana, only 32.3 per cent are 42 Chelydridae explained. If rare taxa are ignored, which may mitigate Dermatemyidae pseudoextinctions, the performance of the TSD hypoth- 36 4543 Kinosternidae esis is still dismal; only 34 per cent of 16 extinctions and D Aves 25 survivals are explained. Our results are also robust to alternate tree topologies and to the inclusion of less- 62 Crocodylinae reliable SDM data (see the electronic supplementary 58–61 Alligatorinae material). Sphenodontidae Even more remarkable is that of the 16 taxa inferred to Dibamidae have had TSD (table 1), only two of them (i.e. Basilemys Gekkota sinuosa and Brachychampsa montana)wentextinct.Incon- Scincidae trast, species with GSD suffered many more extinctions; TSD 28 out of 46 species went extinct (61%). Metatherians Bipedidae (11 species) were entirely wiped out as were all but one Lacertidae ZZ/ZW undetermined species of eutherian (one species of 57 Teiidae Cimolestes is tentatively assumed to have evolved into 53– Gymnophthalmidae Cimolestes simpsoni). Multituberculates did somewhat XX/XY 56 better, with five out of nine species surviving. Only three 48–52 Varanidae out of 10 squamates, all of which are inferred to have Serpentes GSD had GSD, survived into the Palaeocene. The differences Iguania in rates of survival of taxa with TSD as compared with Agamidae those with GSD are statistically significant (p 0.001). uncertain ¼ Chamaeleonidae 4. DISCUSSION Figure 1. Most parsimonious optimization of sex-determining Although we do not have a compelling explanation for mechanisms on a phylogeny of extant tetrapods. Numbers indi- cate where extinct taxa of the Hell Creek Formation attach to this why taxa with TSD fared better than those with GSD tree (see the first column of table 1).
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