Life span, growth, senescence and island syndrome: Accounting for imperfect detection and continuous growth.

Small vertebrates on islands are expected to attain a larger body size, and a greater survival than their mainland counterparts. Comparative studies have questioned whether lizards exhibit this set of adaptations, referred to as the 'island syndrome'. We collected data on 730 individuals the endemic Lilford's lizard Podarcis lilfordi throughout a 10-year period on a small island of the Balearic archipelago (Spain). We coupled a growth function with a capture-mark-recapture model to simultaneously estimate size- and sex-dependent growth rate and survival. To put our results into a wider context, we conducted a systematic review of growth, life span and age at maturity in different Podarcis species comparing insular and mainland populations. We found a low average growth coefficient (0.56 and 0.41 year-1 for males and females to reach an asymptotic size of 72.3 and 65.6 mm respectively), a high annual survival probability of 0.81 and 0.79 in males and females, and a large variability between individuals in growth parameters. Survival probability decreased with body size in both sexes, indicating a senescence pattern typical of long-lived species or in populations with a low extrinsic mortality. Assuming a constant survival after sexual maturity, at about 2 years old, the average life span was 6.18 years in males and 8.99 in females. The oldest animal was a male last captured at an estimated age of ≥13 years and still alive at the end of the study. Our results agree with the predictions of the 'island syndrome' for survival, life span and growth parameters. A comparative analysis of these values across 29 populations of 16 different species of Podarcis indicated that insular lizards grow slower and live longer than their mainland counterparts. However, our data differed from other island populations of the same species, suggesting that island-specific characteristics play an additional role to isolation. Within this study we developed an analytical approach to study the body size-dependent survival of small reptiles. We discuss its applicability to contrast hypotheses on senescence in different sexes of this species, and provide the code used to integrate the growth and capture-mark-recapture models.

Larvae ecology and adult activity of Aedes mariae (Diptera: Culicidae) in a touristic rock-pool area of the Balearic Islands (Western Mediterranean).

Mosquitoes are vectors of several diseases of medical concern such as malaria or dengue and can also negatively affect tourism and the life-quality of the neighbourhood. The species Aedes mariae (Sergent and Sergent, 1903) is a poorly studied mosquito that breeds in rock-pools of the Mediterranean coast. General Linear Mixed Models (GLMM) were used to determine drivers affecting the presence and abundance of this species. Abiotic and biotic factors were recorded in rock-pools with the presence of Ae. mariae sub-adults across a supralittoral area of Majorca Island (Balearic Islands, Spain) from July 2018 to June 2019. We tested how abiotic factors affected the presence of larvae, while the biotic factors were used to check their effect on larvae abundance. human landing collection was also conducted to assess the adult activity of this species. Valuable data were recorded to improve our knowledge about the bioecology of Ae. mariae in a touristic area of the island of Majorca. Salinity and pH were the most explanatory variables for the presence of Ae. mariae larvae. The presence of Posidonia oceanica (L.) Delile 1813 leaves negatively affected the abundance of Ae. mariae larvae while the presence of other fauna enhanced it. Adult females of Ae. mariae were active for 26 min after sunset in June and its host-seeking activity decreased during autumn months. Control methods against this species should be focussed on rock-pools and planning treatments according to tides, waves and precipitation.

Population genetics and phylogeographic history of the insular lizard Podarcis lilfordi (Gunther, 1874) from the Balearic Islands based on genome-wide polymorphic data.

Islands provide a great system to explore the processes that maintain genetic diversity and promote local adaptation. We explored the genomic diversity of the Balearic lizard Podarcis lilfordi, an endemic species characterized by numerous small insular populations with large phenotypic diversity. Using the newly available genome for this species, we characterized more than 300,000 SNPs, merging genotyping-by-sequencing (GBS) data with previously published restriction site-associated DNA sequencing (RAD-Seq) data, providing a dataset of 16 island populations (191 individuals) across the range of species distribution (Menorca, Mallorca, and Cabrera). Results indicate that each islet hosts a well-differentiated population (F ST = 0.247 ± 0.09), with no recent immigration/translocation events. Contrary to expectations, most populations harbor a considerable genetic diversity (mean nucleotide diversity, P i = 0.144 ± 0.021), characterized by overall low inbreeding values (F IS < 0.1). While the genetic diversity significantly decreased with decreasing islet surface, maintenance of substantial genetic diversity even in tiny islets suggests variable selection or other mechanisms that buffer genetic drift. Maximum-likelihood tree based on concatenated SNP data confirmed the existence of the two major independent lineages of Menorca and Mallorca/Cabrera. Multiple lines of evidence, including admixture and root testing, robustly placed the origin of the species in the Mallorca Island, rather than in Menorca. Outlier analysis mainly retrieved a strong signature of genome differentiation between the two major archipelagos, especially in the sexual chromosome Z. A set of proteins were target of multiple outliers and primarily associated with binding and catalytic activity, providing interesting candidates for future selection studies. This study provides the framework to explore crucial aspects of the genetic basis of phenotypic divergence and insular adaptation.

Insular holobionts: persistence and seasonal plasticity of the Balearic wall lizard (Podarcis lilfordi) gut microbiota.

Background: Integrative studies of animals and associated microbial assemblages (i.e., the holobiont) are rapidly changing our perspectives on organismal ecology and evolution. Insular vertebrates provide ideal natural systems to understand patterns of host-gut microbiota coevolution, the resilience and plasticity these microbial communities over temporal and spatial scales, and ultimately their role in the host ecological adaptation. Methods: Here we used the endemic Balearic wall lizard Podarcis lilfordi to dissect the drivers of the microbial diversity within and across host allopatric populations/islets. By focusing on three extensively studied populations/islets of Mallorca (Spain) and fecal sampling from individually identified lizards along two years (both in spring and autumn), we sorted out the effect of islet, sex, life stage, year and season on the microbiota composition. We further related microbiota diversity to host genetics, trophic ecology and expected annual metabolic changes. Results: All the three populations showed a remarkable conservation of the major microbial taxonomic profile, while carrying their unique microbial signature at finer level of taxonomic resolution (Amplicon Sequence Variants (ASVs)). Microbiota distances across populations were compatible with both host genetics (based on microsatellites) and trophic niche distances (based on stable isotopes and fecal content). Within populations, a large proportion of ASVs (30-50%) were recurrently found along the four sampling dates. The microbial diversity was strongly marked by seasonality, with no sex effect and a marginal life stage and annual effect. The microbiota showed seasonal fluctuations along the two sampled years, primarily due to changes in the relative abundances of fermentative bacteria (mostly families Lachnospiraceae and Ruminococcaceae), without any major compositional turnover. Conclusions: These results support a large resilience of the major compositional aspects of the P. lilfordi gut microbiota over the short-term evolutionary divergence of their host allopatric populations (<10,000 years), but also indicate an undergoing process of parallel diversification of the both host and associated gut microbes. Predictable seasonal dynamics in microbiota diversity suggests a role of microbiota plasticity in the lizards' metabolic adaptation to their resource-constrained insular environments. Overall, our study supports the need for longitudinal and integrative studies of host and associated microbes in natural systems.

Chromosome-level genome assembly of Lilford's wall lizard, Podarcis lilfordi (Günther, 1874) from the Balearic Islands (Spain).

The Mediterranean lizard Podarcis lilfordi is an emblematic species of the Balearic Islands. The extensive phenotypic diversity among extant isolated populations makes the species a great insular model system for eco-evolutionary studies, as well as a challenging target for conservation management plans. Here we report the first high-quality chromosome-level assembly and annotation of the P. lilfordi genome, along with its mitogenome, based on a mixed sequencing strategy (10X Genomics linked reads, Oxford Nanopore Technologies long reads and Hi-C scaffolding) coupled with extensive transcriptomic data (Illumina and PacBio). The genome assembly (1.5 Gb) is highly contiguous (N50 = 90 Mb) and complete, with 99% of the sequence assigned to candidate chromosomal sequences and >97% gene completeness. We annotated a total of 25,663 protein-coding genes translating into 38,615 proteins. Comparison to the genome of the related species Podarcis muralis revealed substantial similarity in genome size, annotation metrics, repeat content, and a strong collinearity, despite their evolutionary distance (~18-20 MYA). This genome expands the repertoire of available reptilian genomes and will facilitate the exploration of the molecular and evolutionary processes underlying the extraordinary phenotypic diversity of this insular species, while providing a critical resource for conservation genomics.

Contrasting size-dependent life history strategies of an insular lizard.

In many species with continuous growth, body size is an important driver of life-history tactics and its relative importance is thought to reflect the spatio-temporal variability of selective pressures. We developed a deterministic size-dependent integral projection model for 3 insular neighboring lizard populations with contrasting adult body sizes to investigate how size-related selective pressures can influence lizard life-history tactics. For each population, we broke down differences in population growth rates into contributions from size-dependent body growth, survival, and fecundity. A life table response experiment (LTRE) was used to compare the population dynamics of the 3 populations and quantify the contributions of intrinsic demographic coefficients of each population to the population growth rate (λ). Perturbation analyses revealed that the largest adults contributed the most to the population growth rate, but this was not true in the population with the smallest adults and size-independent fertility. Although we were not able to identify a single factor responsible for this difference, the combination of the demographic model on a continuous trait coupled with an LTRE analysis revealed how individuals from sister populations of the same species follow different life strategies and showed different compensatory mechanisms among survival, individual body growth, and fertility. Our results indicate that body size can play a contrasting role even in closely-related and closely-spaced populations.

Diet composition of the lizard Podarcis lilfordi (Lacertidae) on 2 small islands: an individual-resource network approach.

Despite it is widely accepted that intrapopulation variation is fundamental to ecological and evolutionary processes, this level of information has only recently been included into network analysis of species/population interactions. When done, it has revealed non-random patterns in the distribution of trophic resources. Nestedness in resource use among individuals is the most recurrent observed pattern, often accompanied by an absence of modularity, but no previous studies examine bipartite modularity. We use network analysis to describe the diet composition of the Balearic endemic lizard Podarcis lilfordi in 2 islets at population and individual levels, based on the occurrence of food items in fecal samples. Our objectives are to 1) compare niche structure at both levels, 2) characterize niche partition using nestedness and modularity, and 3) assess how size, sex, season, and spatial location influence niche structure. At population-level niche width was wide, but narrow at the level of the individual. Both islet networks were nested, indicating similar ranking of the food preferences among individuals, but also modular, which was partially explained by seasonality. Sex and body size did not notably affect diet composition. Large niche overlap and therefore possibly relaxed competition were observed among females in one of the islets and during spring on both islets. Likewise, higher modularity in autumn suggests that higher competition could lead to specialization in both populations, because resources are usually scarce in this season. The absence of spatial location influence on niche might respond to fine-grained spatio-temporally distribution of food resources. Behavioral traits, not included in this study, could also influence resource partitioning.

Infestation of small seabirds by Ornithodoros maritimus ticks: Effects on chick body condition, reproduction and associated infectious agents.

Ticks can negatively affect their host by direct effects as blood feeding causing anaemia or discomfort, or by pathogen transmission. Consequently, ticks can have an important role in the population dynamics of their hosts. However, specific studies on the demographic effects of tick infestation on seabirds are still scarce. Seabird ticks have also the potential to be responsible for the circulation of little known tick-borne agents, which could have implications for non-seabird species. Here, we report the results of investigations on potential associations between soft tick Ornithodoros maritimus load and reproductive parameters of storm petrels Hydrobates pelagicus breeding in a large colony in a cave of Espartar Island, in the Balearic archipelago. We also investigated by molecular analyses the potential viral and bacterial pathogens associated with O. maritimus ticks present at the colony. Lower nestling survival was recorded in the most infested area, deep in the cave, compared to the area near the entrance. The parasite load was negatively associated with the body condition of the nestlings. One pool of ticks tested positive for West Nile virus and 4 pools tested positive for a Borrelia species which was determined by targeted nested PCR to have a 99% sequence identity with B. turicatae, a relapsing fever Borrelia. Overall, these results show that further investigations are needed to better understand the ecology and epidemiology of the interactions between ticks, pathogens and Procellariiform species.