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

Origen y mantenimiento de la diversidad fenotípica en poblaciones ibéricas de lagartija colilarga

El estudio del origen y evolución de la divergencia fenotípica, un tema central de la biología evolutiva, ha venido potenciado en los últimos tiempos por el auge de la filogeografía, que aporta los trasfondos filogenéticos y geográficos necesarios para comprender el origen de las diferencias poblacionales. Esta tesis reúne datos filogenéticos y fenotípicos de poblaciones ibéricas de Psammodromus algirus para investigar el origen y mantenimiento de la diversidad fenotípica en esta especie. Los análisis filogenéticos confirman la presencia de dos linajes mitocondriales (oriental y occidental) en la Península Ibérica, y que P. jeanneae y P. manuelae son taxones hermanos y poco diferenciados dentro del linaje occidental. Los experimentos de entorno común revelan procesos de variación contragradiente en ambos linajes. El tamaño de la hembra y la fecundidad se ajustan a la productividad ambiental, con juveniles mayores en sitios menos productivos a modo adaptativo. La incubación a baja temperatura resulta perjudicial para P. algirus, especialmente para los juveniles orientales, lo que podría limitar la expansión hacia el oeste del linaje oriental. Los análisis genéticos revelan cinco clados: W1, W2 (occidentales), E1, E2 y E3 (orientales). Las expansiones geográficas de W2, E2 y E3 han producido diversas zonas de contacto secundario, favoreciendo el flujo génico entre el linaje occidental y E3, cuyas poblaciones constan de lagartijas con un patrón no rayado de coloración dorsal, frente al patrón rayado de las poblaciones de E1 y E2. Experimentos de detección visual demuestran que ambos fenotipos incrementan la capacidad críptica de las lagartijas en sus respectivos hábitats, sugiriendo que los patrones de coloración dorsal han evolucionado en respuesta al riesgo de depredación y que el patrón no rayado ha aparecido de forma convergente en ambos linajes. Así, la ausencia de contacto entre E2 y E3 probablemente se deba a la presencia de barreras ecológicas. [ABSTRACT]The study of the origin and evolution of phenotypic divergence, a central topic of evolutionary Biology, has been lately promoted by the rise of phylogeography, which provides crucial phylogenetic and geographical backgrounds to understand the origin of population differences. This thesis compiles phylogenetic and phenotypic data from Iberian populations of Psammodromus algirus to investigate the origin and maintenance of phenotypic diversity in this species. Phylogenetic analyses confirm the presence of two mitochondrial lineages (eastern and western) in the Iberian Peninsula, and P. jeanneae and P. manuelae being low-differentiated sister taxa within western lineage. Common garden experiments show countergradient variation processes in both lineages. Female size and fecundity are adjusted to environmental productivity, whereas heavier and larger juveniles appear in less productive sites as adaptations. Low-temperature incubation is detrimental for P. algirus, especially for eastern juveniles, a fact that could limit westward expansion of eastern lineage. Genetic analyses reveal five clades: western W1 and W2, and eastern E1, E2 and E3. Geographical expansions of W2, E2 and E3 have yielded several secondary contact zones, promoting gene flow between western lineage and E3, whose populations consist of lizards with a non-striped dorsal pattern, in opposition to the striped dorsal pattern of populations from E1 and E2. Visual detection experiments demonstrate that both phenotypes increase the cryptic capacity of lizards in their respective habitats, suggesting that dorsal coloration patterns have evolved in response to predation risk and non-striped pattern has undergone convergent evolution in previously differentiated eastern and western lineages. Thus, the absence of contact between E2 and E3 is likely a consequence of ecological barrier

Phylogeography of Psammodromus algirus (Lacertidae) revisited: Systematic implications

Relationships among Psammodromus algirus populations from the Iberian Peninsula and North Africa, including recently described P. jeanneae and P. manuelae, were estimated from mitochondrial DNA gene sequences. This enlarged data set confirmed the presence of two divergent eastern and western mitochondrial DNA lineages on the Iberian Peninsula, the distributions for which are separated by a narrow zone of contact across the centre of the Peninsula. Paratypes of P. jeanneae and topotypes of P. manuelae represent southern and northern clades of the western lineage, respectively, making P. algirus paraphyletic. This, together with the low level of allozymic and mitochondrial DNA substructuring within western populations, is not sufficient to retain P. jeanneae and P. manuelae as valid species, and we relegate them to the status of junior synonyms of P. algirus. © 2010 Brill Academic Publishers.Financial support from the projects CGL2007-02744/BOS and CGL2009-11663/BOS was provided 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

Living at the edge: lower success of eggs and hatchlings at lower elevation may shape range limits in an alpine lizard

Studies on range limits clarify the factors involved in the extent of species occurrence and shed light on the limits to adaptation. We studied the effects of elevational variation on the thermal dependence of fitness-related traits (incubation time, hatching rate, and survivorship, size, and condition of hatchlings) to assess the role of incubation requirements in distribution range limits of the alpine endemic Iberolacerta cyreni. We captured gravid females from two core (summit) and two marginal (low-elevation edge) populations, we incubated their eggs at three temperatures (22, 26, and 30 °C), and we monitored phenotypic effects. Viability of eggs and hatchlings decreased, independently of elevation, as incubation temperature increased. Hatching success and embryo survivorship were lower for clutches from low-elevation areas than for those from mountain summits, showing that lizards face difficulties thriving at the low-elevation edge of their range. Such difficulties were partly counterbalanced by faster postnatal growth at lower elevations, leading to increased adult size and higher fecundity. High incubation temperature had detrimental effects also at low-elevation areas, and no elevational variation in the thermal dependence of hatchling traits was detected. We suggest that temperature effects on egg development and the lack of selective pressures strong enough to foster local adaptation at marginal areas, combined with extended egg retention, may contribute to shape the range limits of these alpine oviparous reptiles

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