michelaleonardi Articles, Research

Genetics and ecology do not agree in reconstructing how birds reacted to past climate changes

A new paper in which I took part is now available in Molecular Ecology

Eleanor F. Miller, Rhys E. Green, Andrew Balmford, Pierpaolo Maisano Delser, Robert Beyer, Marius Somveille, Michela Leonardi, William Amos, Andrea Manica
Bayesian Skyline Plots disagree with range size changes based on Species Distribution Models for Holarctic birds
Molecular Ecology, Volume 30, Issue 16 August 2021 Pages 3993-4004

We analysed more than 100 species of Holarctic birds finding that genetics and ecology do not agree in reconstructing how more they reacted to past climatic fluctuations.

Why should we care? The reconstructions compared in our paper (one based on genetic data, the other on ecological modelling) are widely used to assess how well species can react to the ongoing climate emergency.

In our study, we show that when we systematically compare them for a lot of species they tend to tell us quite different stories. This does not mean that they are wrong: different methods are based on different assumptions, and each of them is likely to be missing a small but significant part of the whole story.

So, when we use these methods, the key is interdisciplinarity: integrating into the analyses different lines of evidence help tackle these limitations and get more reliable results.

Article

Eleanor F. Miller, Rhys E. Green, Andrew Balmford, Pierpaolo Maisano Delser, Robert Beyer, Marius Somveille, Michela Leonardi, William Amos, Andrea Manica
Bayesian Skyline Plots disagree with range size changes based on Species Distribution Models for Holarctic birds
Molecular Ecology, Volume 30, Issue 16 August 2021 Pages 3993-4004 https://doi.org/10.1111/mec.16032

Abstract

During the Quaternary, large climate oscillations impacted the distribution and demography of species globally. Two approaches have played a major role in reconstructing changes through time: Bayesian Skyline Plots (BSPs), which reconstruct population fluctuations based on genetic data, and Species Distribution Models (SDMs), which allow us to back-cast the range occupied by a species based on its climatic preferences. In this paper, we contrast these two approaches by applying them to a large data set of 102 Holarctic bird species, for which both mitochondrial DNA sequences and distribution maps are available, to reconstruct their dynamics since the Last Glacial Maximum (LGM). Most species experienced an increase in effective population size (Ne, as estimated by BSPs) as well as an increase in geographical range (as reconstructed by SDMs) since the LGM; however, we found no correlation between the magnitude of changes in Ne and range size. The only clear signal we could detect was a later and greater increase in Ne for wetland birds compared to species that live in other habitats, a probable consequence of a delayed and more extensive increase in the extent of this habitat type after the LGM. The lack of correlation between SDM and BSP reconstructions could not be reconciled even when range shifts were considered. We suggest that this pattern might be linked to changes in population densities, which can be independent of range changes, and caution that interpreting either SDMs or BSPs independently is problematic and potentially misleading.

michelaleonardi Preprints, Research

mtDNA-based reconstructions of change in effective population sizes of Holarctic birds do not agree with their reconstructed range sizes based on paleoclimates

European robin (Erithacus rubecula), picture by Michela Leonardi
European robin (Erithacus rubecula), one of the species analysed in the study.
Picture by Michela Leonardi

A new preprint to which I collaborated was just submitted to BioRxiv: mtDNA-based reconstructions of change in effective population sizes of Holarctic birds do not agree with their reconstructed range sizes based on paleoclimates. The work is led by Eleanor Miller, and was performed under the supervision of Andrea Manica and Bill Amos (University of Cambridge). 

In this article we have studied 102 bird species living in different environments of Eurasia and North America, trying to understand how the climatic changes that occurred after the last glacial maximum (around 21,000 years ago) influenced their demographics . In fact, during the last glacial maximum the climate was much colder, perennial ice covered a large part of the northern hemisphere, and some environments were much more widespread (for example the steppe and cold prairies) while others were much less widespread (for example example forests). For this reason, a difference in the demographic response of species living in different environments could be expected.

Reconstructing the demographics of the past is a very difficult task, there is no method that allows you to do it directly. What can be done is to use different methods that calculate measures that can give us indirect information on what the number of individuals could have been at a given moment. In our article, we used two of these methods, which are based on different data and different assumptions, in order to maximize the amount of information obtained.

The first of these approaches are Bayesian Skyline Plots, which reconstruct the effective population size over time based on mitochondrial DNA. Although the name may be misleading, this measure is not strictly linked to the number of individuals, rather it indicates the degree of genetic variability present in the population. It is based on the assumption that all individuals have the possibility of interbreeding with each other, and the same probability of reproducing: under these conditions, a population with more individuals has a higher genetic variability, for this reason the reconstructions of the effective size are considered informative on demographics. However, they must be interpreted carefully because they can also be influenced by the degree of geographical isolation, by the presence of geographical barriers between groups of individuals, and by many other factors. I will soon be publishing a book chapter on this subject, which clears up some of the more frequent mistakes that can be made in interpreting this kind of information.

The second method is ecological modeling of species distribution (Species Distribution Modelling). This class of methods associates the observations of a species with the environmental or climatic characteristics in which it lives, to reconstruct the potential distribution area both in the present and in the past (or in the future) when simulations of the climate of other periods are available. Again, the size of the distribution area is not directly related to the number of individuals, but this measure is often used as a proxy for demographics assuming that larger distribution areas can support a greater number of individuals.

Our analyses show that when it comes to demographics of the past it is essential not to consider the information drawn from a single method, and to remember that behind every model or measure there are important assumptions that must be tested from time to time. Reality is always more complex than the methods we use to reconstruct it, which is why it is necessary to integrate different approaches in order to be able to have the most complete picture of the situation possible.

Eleanor F. Miller, Rhys E. Green, Andrew Balmford, Robert Beyer, Marius Somveille, Michela Leonardi, William Amos, Andrea Manica

mtDNA-based reconstructions of change in effective population sizes of Holarctic birds do not agree with their reconstructed range sizes based on paleoclimates

During the Quaternary, large climate oscillations had profound impacts on the distribution, demography and diversity of species globally. Birds offer a special opportunity for studying these impacts because surveys of geographical distributions, publicly-available genetic sequence data, and the existence of species with adaptations to life in structurally different habitats, permit large-scale comparative analyses. We use Bayesian Skyline Plot (BSP) analysis of mitochondrial DNA to reconstruct profiles depicting how effective population size (Ne) may have changed over time, focussing on variation in the effect of the last deglaciation among 102 Holarctic species. Only 3 species showed a decline in Ne since the Last Glacial Maximum (LGM) and 7 showed no sizeable change, whilst 92 profiles revealed an increase in Ne. Using bioclimatic Species Distribution Models (SDMs), we also estimated changes in species potential range extent since the LGM. Whilst most modelled ranges also increased, we found no correlation across species between the magnitude of change in range size and change in Ne. The lack of correlation between SDM and BSP reconstructions could not be reconciled even when range shifts were considered. We suggest the lack of agreement between these measures might be linked to changes in population densities which can be independent of range changes. We caution that interpreting either SDM or BSPs independently is problematic and potentially misleading. Additionally, we found that Ne of wetland species tended to increase later than species from terrestrial habitats, possibly reflecting a delayed increase in the extent of this habitat type after the LGM.

bioRxiv 2019.12.13.870410; doi: https://doi.org/10.1101/2019.12.13.870410

michelaleonardi Articles, Research

The female ancestor’s tale: Long‐term matrilineal continuity in a nonisolated region of Tuscany

Lucca_GEarth
The city of Lucca as seen from satellite. Source: Google Earth.

It just come out in American Journal of Physical Anthropology our new paper (behind paywall) The female ancestor’s tale: Long‐term matrilineal continuity in a nonisolated region of Tuscany, in collaboration with Guido Barbujani, Silvia Ghirotto and Francesca Tassi, in Ferrara, and David Caramelli, Stefania Vai and colleagues in Florence. Open-access link to the PDF (read-only).

North-Western Tuscany (roughly Lucca and Massa Carrara provinces) has always been a corridor of exchange between Central and North-Western Italy. The region was disputed between the Etruscans and Ligurians, it has been then conquered by the Romans, and in the following centuries underwent several changes of rulers.

We tried to define if and when such complex history entailed matrilinear discontinuity in the local population. We did so by analysing a portion of the mitochondrial DNA in 119 samples from the region, dated from the Copper age (around 5,000 years ago) the Roman period, the Renaissance, modern-day and including some Etruscan sequences from the whole of Tuscany.

tuscany

Using computer simulations we found out that the better explanation for the genetic diversity in our samples is that they belong to the same population, in continuity through time. This is a quite surprising result since similar degrees of long-term continuity have been mostly observed in isolated areas.

A possible explanation of those results is that either the historical changes observed in north-western Tuscany (conquers, immigration etc.) mainly lead to foreign males arriving and marrying local females. It is also possible that the rulers from outside (Romans, Lombards, French) and the local population did not mix significantly because they were part of different social groups. Whatever the region may be, modern-day Lucca inhabitants appear to be the direct descendants of the women living in the regions millennia ago, teaching us that genetic continuity can not only be found in isolated communities.

Michela Leonardi, Anna Sandionigi, Annalisa Conzato, Stefania Vai, Martina Lari, Francesca Tassi, Silvia Ghirotto, David Caramelli, Guido Barbujani

The female ancestor’s tale: Long‐term matrilineal continuity in a nonisolated region of Tuscany

Objectives: With the advent of ancient DNA analyses, it has been possible to disentangle the contribution of ancient populations to the genetic pool of the modern inhabitants of many regions. Reconstructing the maternal ancestry has often highlighted genetic continuity over several millennia, but almost always in isolated areas. Here we analyze North‐western Tuscany, a region that was a corridor of exchanges between Central Italy and the Western Mediterranean coast.

Materials and methods: We newly obtained mitochondrial HVRI sequences from 28 individuals, and after gathering published data, we collected genetic information for 119 individuals from the region. Those span five periods during the last 5,000 years: Prehistory, Etruscan age, Roman age, Renaissance, and Present‐day. We used serial coalescent simulations in an approximate Bayesian computation framework to test for continuity between the mentioned groups.

Results: Our analyses always favor continuity over discontinuity for all groups considered, with the Etruscans being part of the genealogy. Moreover, the posterior distributions of the parameters support very small female effective population sizes.

Conclusions: The observed signals of long‐term genetic continuity and isolation are in contrast with the history of the region, conquered several times (Etruscans, Romans, Lombards, and French). While the Etruscans appear as a local population, intermediate between the prehistoric and the other samples, we suggest that the other conquerors—arriving from far—had a consistent social or sex bias, hence only marginally affecting the maternal lineages. At the same time, our results show that long‐term genealogical continuity is not necessarily linked to geographical isolation.

Am J Phys Anthropol. 2018;1–10. https://doi.org/10.1002/ajpa.23679 

Read-only pdf