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

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.

Blue Tit
Photo: D. Idiaquez

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.

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Spatially Explicit Evolution of Diversity (SPEED)

Applicant: Peter B. Pearman (Swiss Federal Research Institute WSL)

Co-applicants: Nicolas Salamin (University of Lausanne), Christian Lexer (University of Freibourgh), Niklaus Zimmermann (Swiss Federal Research Institute), Felix Forest (Royal Botanic Gardens, Kew)

Start date: 1 October 2009

Duration: 44 months

Location of research: South Africa, Switzerland

Support: 964, 637 Swiss Franks

Expanded Abstract:

The species environmental niche consists of the biotic and abiotic conditions necessary for long-term persistence and the niche occupies a central place in the development of ecological theories of competition, limiting similarity, and character divergence.  We study interspecific variation in niche characteristics by adopting an evolutionary perspective.  Application of a toolkit used in the disciplines of systematics and evolutionary biology enables us to address how the environmental niche has changed in a family of plants during the diversification of a clade.  We focus on the Restionaceae, a monophyletic family of grass-like plants of which 340 of the 350 species are endemic to southern Africa.  This is a defensible choice because the relative climatic stability of this region during the Pleistocene suggests that these species distributions are currently at equilibrium with climate.  Under accelerating climate change, the capacity of these species for rapid niche evolution will contribute to determining their fate in a landscape where opportunities for successful dispersal to areas of favourable climate may be limited by intervening expanses of unsuitable habitat and the anthropogenic barriers of agriculture, transportation corridors and urbanization. 

We will develop models of niche evolution that serve both for understanding the evolution of extant species diversity and community structure, and for forecasting how diversity and community structure change, given projected climate change and the potential we identify for rapid niche evolution.  We will model characteristics of the ß-niche (habitat-specific, e.g. geology, fire frequency and vegetation type) and ?-niche (climatic), using field-acquired occurrence data for each species. New GIS data layers of fire frequency and geology will be developed.  The relationship between the fundamental and the estimated realized niche will be experimentally evaluated in multiple species.  We will compare in a greenhouse experiment the drought and flooding tolerances of species to their modelled precipitation requirements.  A transplant experiment in the field will help us determine whether species replacement along an elevation and rainfall gradient is driven primarily by fundamental niche requirements or by interspecific competition and, thus, the realized niche.  We will quantify the evolutionary lability of the environmental niche by modelling selected niche parameters over a completely-sampled species-level phylogeny.  This will indicate which parameters have constrained the evolution of the clade and which parameters are associated with differentiation and speciation.  However, working with species-level phylogenies and niche models has formerly entailed assumptions of constant evolutionary rates and equal inheritance of trait variance by new species.  These assumptions will be addressed in population-level analyses of species complexes to determine speciation modes and establish their impacts on the patterns of inheritance of niche variability.  Further studies will estimate using models of trait evolution the variation among clades in rates of niche change.

Using data on species distributions, chorological analyses and niche modeling we will determine current regional species pools.  These will further be stratified into habitat-specific species pools, using field observations, niche models and models of environmental filtering.  Then, using species traits and phylogenetic relationships, we will seek the determinants of community assembly (i.e., the combinations of species from the regional pool that can be combined into communities).  Using the model parameters developed to address the above questions, we will attempt to estimate the possible contribution of rapid evolution of species environmental niches to change in regional species pools and local communities that may accompany altered climate.  These analyses will provide a powerful tool with which to evaluate and predict the response to climate change by multiple, related species and how these changes could impact regional spatial patterns of diversity in the Restionaceae.

The SPEED project developes the tools necessary to address the effects of climate change and the evolutionary response of species to it.  We intend to develop means to convert knowledge on these changes into geographically-explicit patterns of species diversity in the Restionaceae.  We extend the potential impact of our work by including an integrated program for training three Ph.D. students in the evolutionary and ecological modeling techniques that we develop and use during this research.

Publications:

Lexer, C., R. Wüest, S. Mangili, M. Heuertz, K. N. Stölting, P. B. Pearman, F. Forest, N. Salamin, N. Zimmermann, and E. Bossolini. 2014. Genomics of the speciation continuum in an African plant biodiversity hotspot, I: Drivers of population divergence in Restio capensis (Restionaceae). Molecular Ecology 23:4373-4386.

Litsios, G., R. O. Wüest, A. Kostikova, F. Forest, C. Lexer, H. P. Linder, P. B. Pearman, N. E. Zimmermann and N. Salamin. 2014. Differential effect of fire-survival strategy on diversification among a replicated radiation on two continents. Evolution 68:453-465.

Perret, M., A. Chautems, A. O. De Araujo, and N. Salamin. 2013. Temporal and spatial origin of Gesneriaceae in the New World inferred from plastid DNA sequences. Botanical Journal of the Linnean Society 171:61-79.

Lexer, C., K. Stoelting, S. Mangili, F. Forest, E. Bossolini, P. B. Pearman, N. E. Zimmermann and N. Salamin. 2013. ‘Next generation' biogeography: towards understanding the drivers of species diversification and persistence. Journal of Biogeography 40:1013-1022.

D'Amen, M., N. E. Zimmermann, and P. B. Pearman. 2013. Conservation of phylogeographic lineages under climate change. Global Ecology and Biogeography 22:93-104.

Litsios, G., C. Sims, P. B. Pearman, R. O. Wüest, N. E. Zimmermann, and N. Salamin. 2012. Mutualism with sea anemones triggered the adaptive radiation of clownfish. BMC Evolutionary Biology 12:212.

Litsios, G. and N. Salamin. Effects of phylogenetic signal on ancestral state reconstruction. Systematic Biology 61:533-538.

Litsios, G., L. Pellissier, F. Forest, P. B. Pearman, N. E. Zimmermann, and N. Salamin. 2012. Trophic specialization influences the rate of environmental niche evolution in damselfishes (Pomacentridae). Proc. Royal Soc. B. 279:3662-3669.

Broennimann, O., M. Fitzpatrick, P. B. Pearman B. Petitpierre, L. Pellissier and A. Guisan. 2012.  Measuring ecological niche overlap from occurrence and spatial environmental data. Global Ecology and Biogeography 21: 481-497. 

Pearman, P. B., A. Guisan, and N. E. Zimmermann. 2011. Impacts of climate change on Swiss biodiversity: an indicator species approach. Biological Conservation 144:866-875.

Lexer, C. and K. N. Stölting. 2011. Tracing the recombination and colonization history of hybrid species in space and time. Molecular Ecology 20:3701-3704.

Pearman, P. B., M. D'Amen, C. Graham, W. Thuiller, and N. E. Zimmermann. 2010. Within-taxon niche structure: Niche conservatism, divergence and predicted effects of climate change. Ecography 33:990-1003. (Note: first two authors contributed equally to this paper.)

Salamin, N., R. O. Wüest, S. Lavergne, W. Thuiller and P. B. Pearman. 2010. Assessing rapid evolution in a changing environment. Trends in Ecology and Evolution 25:692-698.
 

Evolutionary Niche Dynamics of Invasive Species

Evolutionary Niche dyNamics of Invasive Species (ENNIS)

Applicant: Peter B. Pearman (Swiss Federal Research Institute WSL)

Co-applicant: Nicolas Salamin (University of Lausanne)

Start date: 1 June 2009

Duration: 41 months

Location of research: California, USA and Switzerland

Support: 240,833 Swiss Franks

Expanded Abstract: 

Ecologists seek to understand the factors that lead some exotic plant species to become ecologically dominant and widespread. This attention is justified because these invasive species can alter community composition, impact ecosystem function, affect species' evolutionary trajectories, and lead to species extinctions. Despite these impacts, finding characteristics that are consistently shared by invasive species is difficult. The climatic niche of plants (the climatic conditions under which population growth is positive) potentially facilitates plant invasions. Some groups of invasive plants have native ranges that span large latitudinal gradients.  Other invasive species have experienced shifts of climatic niche during the invasion process.  Niche shifts, both recent and deep in species evolutionary history, likely influence whether immigrant species become established, naturalized and, subsequently, invasive. The evolutionary dynamics of the climatic niche, per se, have seen very little work and there is substantial disagreement over the occurrence, magnitude and rate of climatic niche shifts. These evolutionary niche dynamics are the focus of this proposal.


The main goal of this project is to understand the influence of evolutionary history, especially the history of shifts of the climatic niche, on the invasiveness of exotic species.  Studying the evolutionary history of niche dynamics is not specific to invasive species. Invasive species are a convenient set of model systems (i.e. genera) in which the literature suggests that it is likely that evolution of the climatic niche influences the presence of a detectable ecological quality: invasiveness. Without the criterion of presence of invasives, we could have selected genera at random or used other criteria that would not likely lead the research to have similarly broad interest. In this research we: (a) use a bioinformatics approach to obtain existing data on species distribution and molecular variation within genera that contain invasive species; (b) modify and use existing software to test the degree to which alternative evolutionary models suffice in describing phylogenetic patterns of niche evolution within these genera; (c) test for evolutionary and historical correlates of niche shift and invasiveness by drawing on information from phylogenetic reconstructions, functional traits, and climatic niche characteristics of species.


The first part of the work focuses on collection of (a) ecological, occurrence, and climate data that describe the distribution-climate relationships of species, (b) data on species functional traits, and (c) existing sequence data for phylogeny reconstructions.  We extract species distribution data from online databases and a wide array of other data sources, including the primary literature. We obtain molecular data directly from GenBank.  Additionally, plant tissue for additional sequencing will be collected at national herbaria and botanical gardens.  We model and quantify niche optima and limits using species distribution models and we construct phylogenetic trees of species.  We model the evolution of the climatic niche using existing open-source software, examining potential effects of both selection and random evolution on niche variability. We produce a supertree of the genera and, using both niche and functional trait data, develop general linear models to examine the relationship of these variables to establishment and invasion by exotic species.  Finally, we expand existing software to examine how heterogeneous selection among subclades affects the likelihood of niche shifts and species invasiveness. 

Beyond the importance of understanding the factors that contribute to species invasiveness, this research will contribute to understanding how niche shifts contribute to evolution within genera and affect species distributions. By using genera that include invasive species in Switzerland and elsewhere, the project will contribute to efforts to identify potentially invasive species before they become introduced.  We will gain better understanding of the role of selection and random evolution in niche shifts of invasive species, closely related species, and their ancestors. By helping us to understand the evolutionary history of niche shifts, this research will improve confidence in the use of species distribution models to predict the potential distributions of invasive species.  Finally, understanding evolutionary processes that enable species to expand into new environments may help to predict more accurately the impacts of climate change on plant biodiversity.

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.

D'Amen, M., N. E. Zimmermann, and P. B. Pearman. 2013. Conservation of phylogeographic lineages under climate change. Global Ecology and Biogeography 22:93-104.

Broennimann, O., M. Fitzpatrick, P. B. Pearman B. Petitpierre, L. Pellissier and A. Guisan. 2012.  Measuring ecological niche overlap from occurrence and spatial environmental data. Global Ecology and Biogeography 21: 481-497. 

Engler, R. and 19 additional authors.  2011. 21st century climate change threatens mountain flora unequally across Europe. Global Change Biology 17:2330-2341.

Pearman, P. B., A. Guisan, and N. E. Zimmermann. 2011. Impacts of climate change on Swiss biodiversity: an indicator species approach. Biological Conservation 144:866-875.

Pearman, P. B., M. D'Amen, C. Graham, W. Thuiller, and N. E. Zimmermann. 2010. Within-taxon niche structure: Niche conservatism, divergence and predicted effects of climate change. Ecography 33:990-1003.

Salamin, N., R. O. Wüest, S. Lavergne, W. Thuiller and P. B. Pearman. 2010. Assessing rapid evolution in a changing environment. Trends in Ecology and Evolution 25:692-698.