Integrating genetics, physiology and morphology to study desert adaptation in a lizard species.

Integration of multiple approaches is key to understand the evolutionary processes of local adaptation and speciation. Reptiles have successfully colonized desert environments, that is, extreme and arid conditions that constitute a strong selective pressure on organisms. Here, we studied genomic, physiological and morphological variations of the lizard Liolaemus fuscus to detect adaptations to the Atacama Desert. By comparing populations of L. fuscus inhabiting the Atacama Desert with populations from the Mediterranean forests from central Chile, we aimed at characterizing features related to desert adaptation. We combined ddRAD sequencing with physiological (evaporative water loss, metabolic rate and selected temperature) and morphological (linear and geometric morphometrics) measurements. We integrated the genomic and phenotypic data using redundancy analyses. Results showed strong genetic divergence, along with a high number of fixed loci between desert and forest populations. Analyses detected 110 fixed and 30 outlier loci located within genes, from which 43 were in coding regions, and 12 presented non-synonymous mutations. The candidate genes were associated with cellular membrane and development. Desert lizards presented lower evaporative water loss than those from the forest. Morphological data showed that desert lizards had smaller body size, different allometry, larger eyeballs and more dorsoventrally compressed heads. Our results suggest incipient speciation between desert and forest populations. The adaptive signal must be cautiously interpreted since genetic drift could also contribute to the divergence pattern. Nonetheless, we propose water and resource availability, and changes in habitat structure, as the most relevant challenges for desert reptiles. This study provides insights of the mechanisms that allow speciation as well as desert adaptation in reptiles at multiple levels, and highlights the benefit of integrating independent evidence.

Flowering Phenology Adjustment and Flower Longevity in a South American Alpine Species.

Delayed flowering due to later snowmelt and colder temperatures at higher elevations in the alpine are expected to lead to flowering phenological adjustment to prevent decoupling of peak flowering from the warmest time of the year, thereby favoring pollination. However, even if flowering is brought forward in the season at higher elevations, an elevational temperature gap is likely to remain between the high- and low-elevation populations of a species at the time these reach peak flowering on account of the atmospheric reduction in temperature with increasing elevation. The negative effect of this temperature gap on pollination could be compensated by plastically-prolonged flower life spans at higher elevations, increasing the probability of pollination. In a tightly temperature-controlled study, the flowering phenology adjustment and flower longevity compensation hypotheses were investigated in an alpine species in the Andes of central Chile. The snow free period varied from 7 to 8.2 months over 810 m elevation. Temperatures were suitable for growth on 82-98% of the snow free days. Flowering onset was temporally displaced at the rate of 4.6 d per 100 m increase in elevation and flowering was more synchronous at higher elevations. Flowering phenology was adjusted over elevation. The latter was manifest in thermal sums tending to decrease with elevation for population flowering onset, 50% flowering, and peak flowering when the lower thermal limit for growth (TBASE) was held constant over elevation. For TBASE graded over elevation so as to reflect the growing season temperature decline, thermal sums did not vary with elevation, opening the door to a possible elevational decline in the thermal temperature threshold for growth. Potential flower longevity was reduced by passive warming and was more prolonged in natural populations when temperatures were lower, indicating a plastic trait. Pollination rates, as evaluated with the Relative Pollination Rate index (RPR), when weighted for differences in floral abundance over the flowering season, declined with elevation as did fruit set. Contrary to expectation, the life-spans of flowers at higher elevations were not more prolonged and failed to compensate for the elevational decrease in pollination rates. Although strong evidence for phenological adjustment was forthcoming, flower longevity compensation did not occur over Oxalis squamata´s elevational range. Thus, flower longevity compensation is not applicable in all alpine species. Comparison with work conducted several decades ago on the same species in the same area provides valuable clues regarding the effects of climate change on flowering phenology and fitness in the central Chilean alpine where temperatures have been increasing and winter snow accumulation has been declining.

Extreme Drought Affects Visitation and Seed Set in a Plant Species in the Central Chilean Andes Heavily Dependent on Hummingbird Pollination.

Rising temperatures and increasing drought in Mediterranean-type climate areas are expected to affect plant-pollinator interactions, especially in plant species with specialised pollination. Central Chile experienced a mega drought between 2010 and 2020 which reached an extreme in the austral summer of 2019-2020. Based on intensive pollinator sampling and floral studies we show that the subalpine form of Mutisia subulata (Asteraceae) is a specialised hummingbird-pollinated species. In a two-year study which included the severest drought year, we quantified visitation frequency, flower-head density, flower-head visitation rates, two measures of floral longevity, nectar characteristics and seed set and monitored climatic variables to detect direct and indirect climate-related effects on pollinator visitation. Flower-head density, nectar standing crop and seed set were significantly reduced in the severest drought year while nectar concentration increased. The best model to explain visitation frequency included flower-head density, relative humidity, temperature, and nectar standing crop with highly significant effects of the first three variables. Results for flower-head density suggest hummingbirds were able to associate visual signals with reduced resource availability and/or were less abundant. The negative effect of lower relative humidity suggests the birds were able to perceive differences in nectar concentration. Reduced seed set per flower-head together with the availability of far fewer ovules in the 2019-2020 austral summer would have resulted in a major reduction in seed set. Longer and more intense droughts in this century could threaten local population persistence in M. subulata.