Eco-evolutionary dynamics and macro-evolutionary patterns of multiple signalling

Signals of the condition of individuals directly influence individual fitness through variation in the fitness of chosen mates. They are also targets of sexual selection as females choose males based on variation in traits that may, or may not, be honest signals of male condition.


PI: David López-Idiáquez

Supervisors: Claire Doutrelant, Peter B. Pearman

Collaborators: Vladimir Kaberdin, Maitena San Juan

My lab is currently a collaborator in a study of the effects of pathogens of birds on the signaling of condition in social encounters, such as pairing with mates.  The work is being led by David López Idiáquez, who is a post-doctoral researcher who is working with Doutrelant (CNRS-Montpellier, France) and me. Additionally, Vladimir Kaberdin of the Department of Microbiology and Maitena San Juan, a 4th year student in biology at the UPV, will be collaborating on the analysis of metagenomic DNA from blood and fecal samples. Work in this lab is done in the context of examining the interplay between environment and social signaling systems in a passerine bird.

Sexual and social selection are the main responsible forces for the evolution of a wide array of animal behaviours and morphologies. In many cases, these traits work as signals within a communication context, modulating the outcome of multiple types of interactions (e.g. mating or parent-offspring communication). There is great variability in the number of signals used by the different species. While some of them exhibit rather simple phenotypes with only one signalling trait, others exhibit much more complex ones with multiple signalling traits (Fig. 1). This variability is rather paradoxical, as due to the costs associated to signal expression, we would expect that the individuals will invest all their resources in just one signalling trait to maximize its expression. Therefore, how can we explain the presence of such complex phenotypes?

One of the main ideas proposed to explain the presence of multiple signalling systems is that they are favoured by the spatial and temporal fluctuations in the environmental conditions. In this context, it can be expected that under harsh environments a signal can become too costly for any individual to produce, or under benign conditions, all the individuals can afford to express the signal fully. Under those circumstances, the variance of quality among the signallers could become cryptic and the presence of alternative signals with a different environmental sensitivity will be favoured. Besides, these differences in the expression of multiple signalling traits can also be driven by other factors, such as mating system, that can favour or not the existence and extent of multiple signals. For instance, in highly polygynous mating systems, such as those present in lekking species, there is an enhanced male-male competition that generates the evolution of conspicuous ornaments. However, despite their importance, the effects of the environmental heterogeneity as drivers of the multi-component signalling systems remain overlooked, as most of the experimental, long-term and comparative studies have studied single traits in isolation. It is also important to consider that most of the scientific evidence in this area is male-biased, as there is a lack of studies exploring the role and mechanisms behind female ornamentation in general, and of female multiple signalling in particular. Thus, further research including male and female ornaments is needed to fully comprehend the evolution of the animal signalling systems and to understand the role environmental variation has in that process.

We will tackle this issue by two means: i) we will work on the multiple colourations present in the blue tit (Cyanistes caeruleus), a small (8-11 g) hole-nesting passerine that readily breeds in nest-boxes. First, we will experimentally manipulate their condition by reducing the load of malaria parasites, both in the wild and in captivity, to explore its effects on 5 different coloured traits present in the blue tits. Further, to better understand the mechanisms behind the colouration we will also explore the effects of the treatment on the oxidative status of the birds. Second, we will take advantage of a long-term and individually-based data set including more than 15-years of information about the blue tit colouration, morphology and behaviour. With this information, we will explore the role of the environmental heterogeneity as a driver of the strength and direction of the selection acting on the coloured traits and on their covariation.

The role that this lab plays in the project is to examine more closely the effects of pathogen load on colored traits and their expression.  We will receive collections of blood and feces from the study birds and will extract total genomic DNA.  Then, using universal PCR primers, we will determine the presence/absence of a panel of potential pathogens. These include both viruses, such as avian influenza, and bacteria.  These data should allow us to account for additional variation in signaling traits beyond the potential effects of avian malaria.

Adaptation to Serpentine in a Mediterranean Plant Community

Plants with populations on both serpentine and non-serpentine soils offer an opportunity to study the competing effects of selection and gene flow on adaptation and genomic variation, diversification and homogenization.

Sierra Bermeja near Malaga in southern Spain has extensive areas of serpentine and other ultramaphic soils.

PI:   Peter B. Pearman

Collaborators: Noelia Hidalgo Triana, Andrés V. Pérez, Teresa Navarro de Águila, University of Malaga

Doctoral Student:  Pablo Arrufat


Serpentine soil presents a difficult edaphic environment for most plants for several reasons.  These soils have high concentrations of a variety of heavy metals, a low calcium to magnesium ratio, and tend to have low water content.  These environmental factors have been shown to drive local adaptation to soil in a variety of studies.  In the hills near Malaga, Spain, serpentine outcrops are common and interspersed with areas of non-serpentine soil.  Despite the selective pressure that surely exists for specialization to serpentine environments, a number of plant species have populations on both serpentine and non-serpentine soils, sometimes within sight of each other.  This suggests that there may be strong, contrasting selection among nearly adjacent populations.  This is of interest because adaptation to serpentine has been shown to entail costs, with serpentine genotypes being less able competitors when they occur in non-serpentine environments in reciprocal transplant experiments.

We are developing research that examines the interacting effects of selection and gene flow in several serpentine species, in order to get a broad picture of the response of populations in these communities.  Serpentine and other ultramafic and peridotitic soil is widely distributed in the Sierra Bermeja, not far from the southern Spanish city of Malaga.   We are curious whether gene flow is similar in populations of species that share this heterogeneous environment, and whether any barriers to gene flow are equally effective in the different species.  Some of the species have different subspecies that are typical of one soil or the other, while other species have no recognized morphological differences among populations on different soil types.   We are working with local botanists from Malaga, and we hope to systematically expand our preliminary collections once the pandemic has subsided.  We will then construct ddRADseq libraries at the UPV and contract their sequencing, then probe the data to determine the influences of both gene flow and selection across plant genomes. 

Population Genomics of a Widely-Distributed Perennial

This project seeks to understand historical demography, phylogeography and environmental adaptation in a widespread North American shrub.


PI: Peter B. Pearman

Collaborators: J. Travis Colombus (California Botanical Garden, Claremont, California), Jean-Rémi Trotta and Tyler S. Alioto (Centro Nacional de Análisis Genómico, CNAG, Barcelona)

Start date: April 1, 2014

Duration: ongoing
Research location: Western North America

Support: ad-hoc and discretionary

While mobile animals and plants with substantial dispersal capabilities have the ability to move to follow the changing distributions of suitable climate, many species will have to adapt in situ if they are to persist in the face of climate change. While it is difficult to predict future adaptation, substantial information on the evolutionary history of species in relation to climate can be found by examining genomic variation, current geographic distribution, and morphological variation. This information can be used to inform us about how species potentially respond to the ongoing changing climate. Species with spatial distributions that span substantial environmental variation provide an opportunity to examine how adaptation contributes to maintaining both species breadth and geographic range. In this project we examine geographic variability in genomic variation that has been shaped by both selective and neutral processes, representing both adaptation and demographic history. These genetic patterns reflect distinct processes that are involved in population-level responses to a changing environment. By understanding the history and genomic basis of these responses, we will contribute to understanding how large-scale environmental change may affect future population distribution and adaptation.

Adaptation and evolutionary history in non-model organisms (lacking a reference genome) is increasingly possible through the use of techniques to construct genomic libraries that subsample the genome. We have chosen this approach to develop research on the demographic and evolutionary history of Eriogonum umbellatum (Polygonaceae), a small shrub with bright yellow flowers in western North America. The range of this species extends from the Sierra Nevada almost to the Rocky Mountains, and from the mountains in the southern Mojave Desert to the eastern slopes of the Cascade Range in central Oregon. E. umbellatum is adapted to a variety of arid, semi-arid, and mountainous environments, and occurs on well-drained serpentine and non-serpentine soils. Taxonomists have recognized substantial, though subtle, morphological variation in this species and have described 40 varieties. These varieties vary in the extent of their distribution and the range of environmental conditions they encounter. The high level of taxonomic, morphological, and environmental variation exhibited by the species suggests that rapid adaptive evolution of environmental tolerance characterizes this widely distributed species. Characterizing the genomic basis of this variation, at loci influenced by selection and at others dominated by processes of genetic drift and dispersal, will deepen our understanding of the processes that promote species cohesion or, alternatively, isolate populations and lead to adaptive speciation.

This investigation of population structure, evolutionary history, and environmental adaptation in E. umbellatum builds on previous collaborative work on evolution in Eriogonum and Polygonaceae. In the current work, we have used Genotyping-by-Sequencing to develop a sequenced GBS library and dataset with thousands of bi-allelic SNPs. We have also developed additional genomic resources, including a substantial collection of tissues from over 60 populations, a draft genome using both long-read and Illumina technology, an annotated transcriptome, and a custom bioinformatics pipeline. We are currently examining the diversity within E. umbellatum and some closely related congeners and other relatives in an effort to determine the species boundaries and monophyly of this taxon. Our SNP data encompass about 30 additional species in the genera Eriogonum and Chorizanthe. Our initial analyses indicate that species-level designation is needed for some taxa that are currently distinguished at the varietal level.

Once we know species boundaries, we will examine intraspecific structure and identify potential loci under environmental selection. This will serve as the basis for modeling genome-environment associations and, subsequently, the geographic displacement of suitable environmental conditions as climate change progresses. To do this, we will develop ddRADseq libraries at UPV. After sequencing, additional modeling will address the demographic and phylogeographic history of the species through the Neogene. We intend to identify clusters of populations that share a common demographic and evolutionary history. With this information, we will examine the environmental distribution of potentially adaptive loci using targeted sequencing methods.

Relevant Publications

Kostikova, A., N. Salamin and P. B. Pearman. 2014. The role of climatic tolerances and seed traits in reduced extinction rates of temperate Polygonaceae. Evolution 68:1856-1870.

Kostikova, A., G. Litsios, S. Burgy, L. Milani, P. B. Pearman, and N. Salamin. 2014. Scale-dependent adaptive evolution and morphological convergence to climate niche in the Californian eriogonoids (Polygonaceae). Journal of Biogeography 41:1326-1337.

Kostikova, A., G. Litsios, N. Salamin, and P. B. Pearman.  2013. Linking life history traits, ecology and niche breadth evolution in the North American eriogonoids (Polygonaceae). American Naturalist 182:760-774.