Life-history traits of two Mediterranean lizard populations: a possible example of countergradient covariation

Received: 1 October 2011 / Accepted: 27 September 2012 / Published online: 18 October 2012The trade-off between clutch and offspring size, which is a central topic in life-history research, is shaped by natural selection to maximize the number of surviving offspring, but it also depends on the resources available for reproduction. Conspecific populations living in different environments may differ in adult body size, clutch mass, clutch size, offspring size, and/or post-natal growth rates, due either to phenotypic plasticity or to local adaptation. Here, we compare these traits and their relationships between two populations of the lizard Psammodromus algirus separated by a 600-m altitudinal gradient. We used a common garden design to control incubation temperature and food availability, with two different feeding treatments. Females were larger at the high-elevation site. Although SVL-adjusted clutch mass did not differ between populations, high-elevation females laid more but smaller eggs than low-elevation ones. Hatchlings were larger at lower elevation. Our common garden experiment revealed that low-elevation hatchlings grewfaster than high-elevation hatchlings under both feeding treatments. However, higher food availability at higher altitude allows high-elevation lizards to grow faster and attain larger adult sizes, especially in the case of females. The two key adaptations of low-elevation lizards, large eggs and hatchlings and the ability to grow rapidly after hatching, are likely to enhance survival in low-productivity Mediterranean lowlands. Our data support the hypothesis that the reproductive strategies of these populations provide an example of countergradient variation, because the genotypes that encode for fast growth and large body size occurred in low food availability habitats where juveniles grewslowly and attained small adult sizes.This paper is a contribution to the projects CGL2007-60277/BOS and CGL2010-17928/BOS funded by the Spanish Ministry of Education and Science, and to the International Campus of Excellence (CEI Campus Moncloa) launched by Complutense University of Madrid (UCM) and Spanish Research Council (CSIC).Peer reviewe

There is more to the picture than meets the eye: adaptation for crypsis blurs phylogeographical structure in a lizard

Aim: We examined dorsal coloration in and genetic relationships among Iberian populations of the lizard Psammodromus algirus to determine the extent to which the current distribution of phenotypic variation is correlated with phylogeographical history or local environmental conditions. Location: Iberian Peninsula, western Palaearctic.Methods: We sequenced mitochondrial DNA (ND4 and adjacent tRNAs genes) in 36 populations, and seven microsatellite loci in eight representative populations. In 23 populations, lizards were classified according to the presence and intensity of a dorsal striped pattern, the heritability of which was estimated by means of mother–offspring regressions. To determine whether colour pattern is an adaptation for crypsis, we compared the time taken by humans to detect striped and unstriped lizards in different environments.Results: The analysis of mtDNA revealed an ancient split between a western clade, subdivided into south- and north-western haplogroups, and an eastern clade with central, south-eastern and eastern haplogroups. In contrast, nuclear markers showed a post-glacial admixture of central and western haplogroups, with the central haplogroup apparently isolated from the rest of its clade. This was consistent with variation in the dorsal striped pattern, a heritable phenotypic trait: central and western lizards were unstriped, whereas eastern lizards were striped. We then suggest that dorsal coloration promotes crypsis: in eastern locations detection times were longer for striped than for unstriped lizards, whereas the opposite was true in western and central locations.Main conclusions: Our results indicate that natural selection for crypsis may promote not only divergence within clades, as suggested by the apparent isolation between unstriped central lizards and striped members of eastern haplogroups, but also admixture between them. We conclude that ecologically driven selection is crucial for understanding the phylogeographical background of phenotypic variation, because recent adaptation to the environment can blur the effects of ancestral isolation.This study is a contribution to projects CGL2010-17928/BOS and CGL2013-41642-P, funded by the Spanish Ministry of Education and SciencePeer reviewe

Albiglutide and cardiovascular outcomes in patients with type 2 diabetes and cardiovascular disease (Harmony Outcomes): a double-blind, randomised placebo-controlled trial

Background: Glucagon-like peptide 1 receptor agonists differ in chemical structure, duration of action, and in their effects on clinical outcomes. The cardiovascular effects of once-weekly albiglutide in type 2 diabetes are unknown. We aimed to determine the safety and efficacy of albiglutide in preventing cardiovascular death, myocardial infarction, or stroke. Methods: We did a double-blind, randomised, placebo-controlled trial in 610 sites across 28 countries. We randomly assigned patients aged 40 years and older with type 2 diabetes and cardiovascular disease (at a 1:1 ratio) to groups that either received a subcutaneous injection of albiglutide (30–50 mg, based on glycaemic response and tolerability) or of a matched volume of placebo once a week, in addition to their standard care. Investigators used an interactive voice or web response system to obtain treatment assignment, and patients and all study investigators were masked to their treatment allocation. We hypothesised that albiglutide would be non-inferior to placebo for the primary outcome of the first occurrence of cardiovascular death, myocardial infarction, or stroke, which was assessed in the intention-to-treat population. If non-inferiority was confirmed by an upper limit of the 95% CI for a hazard ratio of less than 1·30, closed testing for superiority was prespecified. This study is registered with ClinicalTrials.gov, number NCT02465515. Findings: Patients were screened between July 1, 2015, and Nov 24, 2016. 10 793 patients were screened and 9463 participants were enrolled and randomly assigned to groups: 4731 patients were assigned to receive albiglutide and 4732 patients to receive placebo. On Nov 8, 2017, it was determined that 611 primary endpoints and a median follow-up of at least 1·5 years had accrued, and participants returned for a final visit and discontinuation from study treatment; the last patient visit was on March 12, 2018. These 9463 patients, the intention-to-treat population, were evaluated for a median duration of 1·6 years and were assessed for the primary outcome. The primary composite outcome occurred in 338 (7%) of 4731 patients at an incidence rate of 4·6 events per 100 person-years in the albiglutide group and in 428 (9%) of 4732 patients at an incidence rate of 5·9 events per 100 person-years in the placebo group (hazard ratio 0·78, 95% CI 0·68–0·90), which indicated that albiglutide was superior to placebo (p<0·0001 for non-inferiority; p=0·0006 for superiority). The incidence of acute pancreatitis (ten patients in the albiglutide group and seven patients in the placebo group), pancreatic cancer (six patients in the albiglutide group and five patients in the placebo group), medullary thyroid carcinoma (zero patients in both groups), and other serious adverse events did not differ between the two groups. There were three (<1%) deaths in the placebo group that were assessed by investigators, who were masked to study drug assignment, to be treatment-related and two (<1%) deaths in the albiglutide group. Interpretation: In patients with type 2 diabetes and cardiovascular disease, albiglutide was superior to placebo with respect to major adverse cardiovascular events. Evidence-based glucagon-like peptide 1 receptor agonists should therefore be considered as part of a comprehensive strategy to reduce the risk of cardiovascular events in patients with type 2 diabetes. Funding: GlaxoSmithKline

Variación altitudinal de las estrategias vitales de dos poblaciones ibéricas de lagartija colilarga "Psammodromus algirus"

Las estrategias vitales se definen como el conjunto de rasgos que determinan las variaciones en fecundidad y supervivencia a lo largo de la vida de los organismos. Estas estrategias han sido moduladas por la selección natural para maximizar el éxito reproductivo en un ambiente determinado. Por lo tanto, en especies con rangos de distribución amplios lo esperable sería encontrar diferencias entre poblaciones en las estrategias vitales debidas a las distintas características ambientales de cada población. Estas diferencias ambientales también pueden promover variación en rasgos morfológicos y comportamentales. En esta Tesis vamos a estudiar las diferencias en las características fenotípicas –de estrategias vitales, comportamiento antidepredatorio y morfología– de dos poblaciones de Psammodromus algirus (una lagartija endémica del oeste de la cuenca mediterránea) a lo largo de un gradiente altitudinal. Las hembras de la localidad de llanura, para asegurar que sus descendientes puedan sobrevivir bajo las severas condiciones de las llanuras xéricas mediterráneas, se ven forzadas a invertir más por descendiente que las hembras de la localidad de montaña (donde la abundancia de alimento es mayor y la intensidad de la sequía estival es menor), lo que conlleva una reducción del número de descendientes. Por otro lado, los recién nacidos de la localidad de llanura son capaces de crecer más rápido en distintas condiciones de disponibilidad trófica, y de inactivarse si las condiciones son demasiado adversas. Sin embargo, los juveniles de la localidad de montaña, gracias a la abundancia de alimento en su ambiente, son capaces de crecer rápido y alcanzar tallas mayores como adultos, especialmente en caso de las hembras. La diferencia en la estructura del hábitat entre las dos poblaciones ha modulado el comportamiento antidepredatorio de las hembras grávidas; en la localidad de llanura (con menor disponibilidad de refugios) la hembras grávidas hacen carreras más cortas y lentas y pasan un mayor porcentaje de tiempo en las proximidades de los refugios. En cuanto a los machos, debido probablemente a la mayor intensidad de las presiones de selección sexual en la localidad de llanura, presentan diferencias morfológicas. Los machos de la localidad de llanura poseen patas más largas, más poros femorales y una coloración sexual más pronunciada, lo que contribuiría a optimizar la comunicación intraespecífica bajo condiciones ambientales de mayor sequedad, temperaturas más elevadas y, posiblemente, mayor visibilidad. En esta Tesis hemos encontrado que la variación fenotípica existente parece maximizar el éxito reproductivo en las dos poblaciones estudiadas, poniendo de manifiesto su capacidad para adaptar su biología reproductiva y estrategias vitales a la variación de las condiciones ambientales a lo largo de un gradiente altitudinal. [ABSTRACT]Abstract Life-history strategies may be defined as co-adapted suites of traits that determine the variations in fecundity and survivorship throughout the life of organisms. These strategies have been shaped by natural selection to maximize reproductive success in a particular environment. In widely distributed species, it is therefore expected to find interpopulation differences in life-history strategies, due to the particular environmental conditions experienced by different populations. Here, we analyze the differences in phenotypic traits –life-history strategies, antipredatory behavior, and morphology– between two populations of the Large Psammodromus Psammodromus algirus (a lacertid lizard from the western Mediterranean basin) separated by 600-700 m along an elevational gradient. Low-elevation females, in order to ensure the survival of their offspring under the harsh conditions of xeric Mediterranean lowlands, are constrained to perform a higher per-offspring investment than females from the high-elevation site, where food availability is higher and the intensity of the summer drought is lower; this implies trading larger clutches for larger offspring. On the other hand, low-elevation hatchlings are able to grow faster under different conditions of food availability both in the field and under a ‘common-garden’ design, and they are also able to remain inactive if the conditions are too harsh to compensate the metabolic and predation-risk costs of activity. However, high-elevation juveniles, due to higher food abundance at the highelevation site, are able to grow faster and attain a larger size as adults, especially in the case of females. Between-populations differences in habitat structure may have shaped the antipredatory behavior of gravid females; at the low-elevation site, with lower refuge availability, gravid females run more slowly, they cover shorter distances, and they spend more time sheltered or near refuges. Males, probably due to the higher intensity of sexual selection pressures at the low-elevation site, also show morphological differences. Low-elevation males have longer hind limbs, more and larger femoral pores, and a more intense nuptial coloration, which might contribute to optimize intraspecific communication in an environment with drier, hotter conditions (and probably with higher visibility). To summarize, in this PhD thesis we argue that current phenotypic variation seems to maximize reproductive success in the two populations studied, revealing their ability to adjust their reproductive characteristics and life-history strategies to the challenges posed by environmental variation along a Mediterranean elevational gradient

Effects of Caudal Autotomy on Postnatal Growth Rates of Hatchling Psammodromus algirus

Tail autotomy has clear advantages regarding predator escape, but it also has several associated costs (i.e., impaired locomotion, loss of social status, and reduced growth and reproductive output). We examined the costs of severe autotomy on growth rates of hatchlings of the lacertid lizard sammodromus algirus during the first weeks of postnatal development. Hatchlings from two populations in central Spain were autotomized on the fifth day after hatching and kept in common garden conditions for 35 days when they were measured again. Hatchlings from both populations, independently of the autotomy treatment, did not differ in the mass gained during the experiment. However, there were differences in body growth between tailless and tailed hatchlings; tailless hatchlings grew at a slower rate than tailed ones, after controlling for the effects of body condition at the onset of the experiment and the resources assimilated. Moreover, independently of their population of origin, hatchlings that invested more in body growth also invested more in regenerating their tails, and no trade-offs were apparent. Because hatchlings were housed in common garden conditions, this result could be attributable to differences in individual capacity to obtain and assimilate resources.This paper is a contribution to the projects CGL2007-60277/BOS and CGL2010-17928/BOS, funded by the Spanish Ministry of Education and Science, and to the International Campus of Excellence (CEI Campus Moncloa) launched by Complutense University of Madrid (UCM) and Spanish Research Council (CSIC).Peer reviewe

Sexual dimorphism and interpopulation differences in lizard hind limb length: locomotor performance or chemical signalling?

Received 16 March 2011; revised 11 May 2011; accepted for publication 11 May 2011Intraspecific variation in morphology has often been related to fitness differences through its effects on performance. In lizards, variation in hind limb length can be shaped by natural selection for increased locomotor performance, sexual selection on the number or size of femoral pores involved in chemical signalling, or both. Here, we analyse the selective forces involved in sexual dimorphism and differences in hind limb length between two populations of Psammodromus algirus living at different elevation. Males were more robust and had longer hind limbs and limb segments than females, and low-elevation lizards had longer limbs than high-elevation lizards. However, differences in locomotor performance were small and non-significant, making natural selection for faster runs an unlikely explanation for the observed pattern. On the other hand, males had more femoral pores than females, and lizards had more pores at lower elevation, although the difference was significant only for males (which invest more in chemical signalling). In males, the number of pores, which remains constant along a lizard's life, was not correlated with hind limb length. However, femur length was positively correlated with mean pore size, allowing low-elevation males to have larger than expected pores, which could increase the effectiveness with which they spread their signals in a dry and warm habitat where chemicals become volatile rapidly. Also, saturation of the sexual coloration of the head was higher for low-elevation males, suggesting that sexual selection pressures may be more intense. Overall, our results indicate that sexual selection plays a significant role in shaping intraspecific variation in hind limb length.This paper is a contribution to projects CGL2007-60277/BOS and CGL2010-17928 funded by the Spanish Ministry of Education and Science.Peer reviewe

Phenotypic responses to incubation conditions in ecologically distinct populations of a lacertid lizard: a tale of two phylogeographic lineages

We experimentally studied the effects of genetic legacy (eastern vs. western phylogeographic lineage) and population of origin (lowland vs. highland) on the sensitivity of lizard embryos and juveniles to incubation temperature and moisture among four populations of the lacertid Psammodromus algirus. Incubation time was longer at lower temperature, increased slightly at higher moisture, and shorter for highland than for lowland females. Eggs incubated at 24°C produced larger, heavier and shorter tailed hatchlings than those incubated at 32°C. Western juveniles survived better during their first month of life than eastern ones, and juveniles incubated at 32°C survived better than those incubated at 24°C; survivorship was lowest for 24°C hatchlings from the eastern, lowland population. Because juveniles incubated at 32°C grew more rapidly, after 1 month they had compensated their initial size disadvantage. Juveniles incubated at 80% moisture were larger and/or heavier than those incubated at 10% moisture both at hatching and after 1 month. Our results show that although incubation temperature was the main source of phenotypic variation, not all its effects were evident at hatching. Because western juveniles were more tolerant to incubation at low temperature than eastern ones, we suggest that such differences may have limited the westward expansion of the eastern lineage.This study is a contribution to projects CGL2007-60277/BOS and CGL2010-17928/BOS, funded by the Spanish Ministry of Education and Science.Peer reviewe

Differences in males’ chemical signals between genetic lineages of the lizard Psammodromus algirus promote male intrasexual recognition and aggression but not female mate preferences

Interpopulational variation in sexual signals may lead to premating reproductive isolation and eventually may result in speciation. We explored the role of chemical cues secreted by the femoral glands of male lizards Psammdoromus algirus in chemosensory recognition between two distinct genetic lineages from Central Spain. We hypothesized that if there were differences in chemical sexual signals between lineages, these may result in differential recognition and mate preferences. This might lead to reproductive isolation, which would allow the observed morphological and genetic differences between lineages. Our results showed that males of each lineage secreted a singular mixture of compounds in their femoral secretions. However, females were apparently not able to discriminate the lineage of males by chemosensory cues or, alternatively, this discrimination may not be important for females. Moreover, females did not select or reject areas scent marked by males of their own vs. the other lineage. However, previous studies suggest that females might prefer scent of males with particular chemical characteristics that show interindividual variability but do not vary between lineages. Similarly, males did not discriminate between the scents of females of the two lineages, although they had greater chemosensory responses to scents of larger females. In contrast, males clearly discriminated the lineage of other males based on their scents alone, showing chemosensory and aggressive responses that were higher to scents of males of the other lineage. If males of the opposite lineage were more prone to be detected and excluded from a male territory due to their differences in chemical signals, this may probably impede the access of males of one lineage to females of the opposite lineage. This might result in reproductive isolation between lineages. We suggest that the current genetic divergence observed between lineages of P. algirus lizards may be mediated by intrasexual relationships among males, but not by female mate preferences. Significance statement Sexual signals often vary geographically to maximize their efficiency in communication under local conditions. Such variation may, however, affect recognition between individuals of different populations, resulting in reproductive isolation and speciation. We studied two populations (lineages) of a lizard with genetic and morphological differences. We found clear inter-lineage variation in chemical profiles of sexual signals of males. However, females did not recognize these differences by chemosensory cues and did not prefer or reject areas scent-marked by males of the two lineages. In contrast, males recognized and responded more aggressively toward scent of males of the opposite lineage. This might impede access of males of one lineage to females of the other. We suggest that the observed differences between lineages may result from partial reproductive isolation, which can be mediated by agonistic interactions between males rather than by female mate preferences.Financial support was provided by the Spanish’s Ministerio de Economía y Competitividad projects MICIIN-CGL2010-17928/BOS and MINECO CGL2014-53523-P.Peer Reviewe

Intraspecific variation of reproductive traits in a Mediterranean lizard: clutch, population, and lineage effects

Widely distributed terrestrial ectotherms from the southern European peninsulas show patterns of subdivision (related to isolation in temperate refugia) that allow us to test the relative importance of phylogeographic lineage, population of origin and familial effects as sources of variation for life-history traits. We collected gravid females from 15 geographically separated populations of the lacertid lizard Psammodromus algirus, a widely distributed species with well differentiated eastern and western lineages. We incubated eggs under two treatments of constant (28 C) and fluctuating (28 ± 4 C) temperature, and we examined clutch, population, and lineage effects on several traits of females, eggs, and hatchlings. Incubation time was mainly explained by differences between lineages, but it was also influenced by population and female effects. Within each lineage, incubation was shorter at cooler and wetter sites, and for a given climate it was shorter for eastern than for western populations, suggesting that countergradient variation has evolved independently in the two lineages. Female size, clutch size, and relative fecundity were primarily influenced by inter-population differences, a pattern that seemed attributable to environmental differences in productivity, because mean female size was positively correlated with a gradient of increasing precipitation and decreasing temperature. Clutch size was mainly, but not entirely, dependent on female SVL, suggesting both a proximate effect of local conditions and intrinsic differences among populations. Females from drier and warmer sites produced larger hatchlings. Mean egg mass was mainly determined by familial effects. Eggs incubated at a constant temperature hatched earlier than did their siblings incubated at fluctuating temperatures, a fact that could be explained by considering that in Mediterranean environments developmental rate might increase at a lower speed above average incubation temperature than it does decrease below it.This study is a contribution to projects CGL2007-60277/BOS and CGL2010-17928/BOS, funded by the Spanish Ministry of Education and Science.Peer reviewe