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Integrative and Comparative Biology Integrative and Comparative Biology, Volume 58, Number 6, Pp Integrative and Comparative Biology Integrative and Comparative Biology, volume 58, number 6, pp. 1086–1097 doi:10.1093/icb/icy119 Society for Integrative and Comparative Biology INVITED PAPER Effects of Climate and Latitude on Age at Maturity and Longevity of Lizards Studied by Skeletochronology 1 Facundo Cabezas-Cartes, Jorgelina M. Boretto and Nora R. Ibargu¨engoytıa Downloaded from https://academic.oup.com/icb/article-abstract/58/6/1086/5126835 by guest on 15 December 2018 Laboratorio de Ecofisiologıa e Historia de Vida de Reptiles, INIBIOMA, Universidad Nacional del Comahue, CONICET, Quintral 1250, San Carlos de Bariloche (8400), Rıo Negro, Argentina 1E-mail: [email protected] Synopsis Longevity and age at maturity are key life-history traits, directly linked to fitness attributes such as survival and reproductive output. It has been proposed that these traits are strongly influenced by environmental factors, such as temperature, seasonality, and precipitations, which determine the existence of a continuum of life-histories that goes from the “slow” life histories characterized by late maturity and high longevity of cold and highly seasonal climates to the “fast” life histories characterized by early maturity and low longevity, typical of the tropical climates. However, large- scale studies that address these topics in lizards are scarce and most of them are based on heterogeneous data, which may overlook the real patterns. Using skeletochronology, we studied age at maturity and longevity of two species of Phymaturus lizards, Phymaturus aguanegra from the Andes and Phymaturus zapalensis from the Patagonian steppe (Argentina). Then, we confronted longevity and age at maturity in these species with published skeletochronology- based data on 46 other lizard species to examine possible association of these life-history traits with latitude and mean annual temperature, thermal amplitude, and precipitations. Both Phymaturus species showed late sexual maturity (7 and 8–9 years, respectively) and high longevity (16 and 14–15 years, respectively) in coincidence with the other species of the genus studied up to date. The phylogenetic comparative analysis revealed that the most important variable in the determination of longevity patterns in the species studied was latitude: at higher latitudes lizards tend to live longer. In contrast, age at sexual maturity was dependent on mean annual temperature most, especially in males, as lizards from hotter climates mature earlier than lizards from cold sites. Introduction and Angilletta 2004; Horvathova et al. 2013). For Environmental gradients of temperature, thermal example, at high latitudes, lizards’ activity seasons amplitude (TA), precipitation, and photoperiod are are short, and populations characterized by slow known to affect many life-history traits of ecto- growth, late sexual maturity, and high longevity therms (Shine 2005) such as longevity and age at (Piantoni et al. 2006; Kubisch et al. 2012). sexual maturity (ASM). Specifically, temperature Furthermore, high latitudes are associated with cool has a great influence over physiological performance environmental temperatures and, consequently, a (Huey and Stevenson 1979; Pinch and Claussen slow pace-of-life, as shown for diverse ectotherms 2003; Angilletta 2006; among others) and, conse- such as fishes and flies (Valenzano et al. 2006; quently, growth rates (Zug et al. 2001), age and Conti 2008). Besides, other climatic factors such as size at sexual maturity (Adolph and Porter 1996; precipitations can also affect indirectly life-history Niewiarowski 2001), reproductive frequency traits through their effects over food availability (Olsson and Shine 1999; Ibargu¨engoytıa and (Dunham et al. 1988). Casalins 2007), and the number and size of offspring The ASM is one of the most important life-history (Winkler et al. 2002; Shine 2005; Angilletta 2009). traits because it is correlated with fitness and it is However, in cold-climate species which undergo usually more sensitive to natural selection than any long periods of brumation, activity times also be- other life-history trait (Stearns 2000). Life-history come of paramount importance in the determination theory predicts that late sexual maturity at a greater of life-history traits (Adolph and Porter 1993; Sears size is favored by an increase in fecundity or survival Advance Access publication October 11, 2018 ß The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. Longevity and age at maturity in Sauria 1087 of offspring (Roff 1992; Kozlowski et al. 2004; group as they have a simple bone structure with Arendt 2011). This is a common pattern in lizards low vascularization [except for large varanids that inhabiting cold climates, as low environmental tem- exhibit bone vascular canals (De Buffrenil et al. peratures reduce the metabolic rate, retarding 2008)] in addition to low intracortical remodeling growth, and age at maturity (Andreone and and infrequent supplementary marks (Castanet Guarino 2003). Ecological factors such as predation 1994). Specifically, lizards from cold-temperate pressure can also affect age at maturity (Scharf et al. regions are better study models than those inhabiting 2015), and in environments with high predation the tropics, since their growth rings are more evident pressures it is expected that natural selection would as a result of the reduction in metabolic activity favor the early reproduction at lower ages in order to produced by the low temperatures during cold sea- avoid mortality before procreation. sons (Castanet et al. 1993). Downloaded from https://academic.oup.com/icb/article-abstract/58/6/1086/5126835 by guest on 15 December 2018 Longevity is a highly variable trait, influenced by In this study, we present original age and growth intrinsic and extrinsic factors (Scharf et al. 2015). data of two species of Phymaturus lizards Among the intrinsic factors, the most important (Liolaemidae) from high altitudes in the central are the accumulation of mutations (Hughes and Andes (Phymaturus aguanegra from the palluma Reynolds 2005), the pleiotropic genes that encode phylogenetic group) and high latitudes in the phenotypes that are beneficial early in life but encode Patagonian steppe (Phymaturus zapalensis from the other traits that are harmful later in life (Ljubuncic patagonicus phylogenetic group) of Argentina. and Reznick 2009), and the generation of harmful Phymaturus is a genus of viviparous, saxicolous, metabolic by-products (Sohal 1986; Wilkinson and and predominantly herbivorous lizards which South 2002). However, the effects of these intrinsic includes species that live along a latitudinal and al- factors in species that experience indeterminate titudinal gradient in the Andes and Patagonia of growth like reptiles have been questioned with the Argentina and central Chile (Cei 1986; Debandi findings of the existence of negative senescence, et al. 2012; Morando et al. 2013). The species studied which states that mortality rate declines with age in up to date present slow life histories characterized by adult individuals (Vaupel et al. 2004), in some liz- high ASMs (6–9 years old) and medium to high lon- ards species (Tinkle and Ballinger 1972; Tinkle et al. gevities (12–20 years old; Piantoni et al. 2006; 1993; Heulin et al. 1997), posing more importance to Boretto et al. 2015, 2018; Cabezas-Cartes et al. extrinsic factors in the determination of longevity 2015), which suggest that, among lizards, liolaemids patterns. The most influential extrinsic factor on lon- present extraordinary high longevities and ASMs in gevity is mortality, either caused by predation, star- relation to their body size. The results obtained for vation, and/or parasites and diseases (Healy et al. these Phymaturus species are integrated with data of 2014; Valcu et al. 2014). Mortality associated with wild populations of 46 lizard species, also studied by predation and competition would be lower at high skeletochronology, in order to discuss the influence latitudes, since it has been demonstrated that biotic of environmental conditions in two pivotal life- interactions such as predation and competition are history traits such as ASM and longevity, and com- significantly reduced at high latitudes (Schemske pare these life-history traits between liolaemids and et al. 2009). Also, at high latitudes, seasonality is others saurians. strong, shortening the annual activity times which has been shown to have positive effects on survival Materials and methods rate (Adolph and Porter 1993). Moreover, in highly Age and growth of P. aguanegra and P. zapalensis seasonal climates lizards hibernate and during this period metabolism decreases significantly, reducing Specimens mutation rates and oxidative damage. Hence, both For the present study we used museum specimens of intrinsic and extrinsic mortality are reduced in cold the herpetological collection of the Department of regions and high latitudes, which would lead to pro- Zoology at the Centro Regional Universitario longed life cycles (Scharf et al. 2015). Bariloche (CRUB), Universidad Nacional del In order to describe the life-history of a species, it Comahue. Specifically, we analyzed 2 offspring, 14 is essential to estimate two pivotal life-history juveniles, 11 adult females, and 11 adult males of traits—ASM and longevity. In this sense, skeleto- P. aguanegra
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