Learning to prefer the smell and sight of males

My latest paper, on the ontogeny of female preferences for multiple signals, has recently been published in Animal Behaviour (link to it is here)

It is a paper about a study I did during my first postdoctoral project, with Gil Rosenthal, who is a co-author on this paper. Work by Gil and those in his lab focuses on the behaviour and biogeography of swordtail fish (check out the lab webpage), which are live bearing poecillids, living in the Sierra Madre Oriental in Mexico. The males of many of these species have extended caudal fins, which look a bit like swords, hence their name. Females of some species show preferences for these swords, sometimes even if the males of their own species don’t show this sword! They also show other visual traits, used in display to females, such as the dorsal fin, and the pattern of bars.

Males not only show off these visual features during courtship to females, they also use olfactory cues. In a very cool experiment (paper can be found here), Gil and co-workers show that males release these olfactory cues in their urine, during a courtship display upstream of the female.

Even though we don’t know as yet what the chemical nature of these signals are, these olfactory cues are species specific, as figured out by a lot of behavioural trials by several people (cited in my & Gil’s paper). Comparing female preferences for olfactory cues and the visual image of each species, females choose more often for males of their own species on the basis of olfactory cues than on the visual image.

In our recent paper, we report a study in which we compared the ontogeny of female preferences for olfactory cues and visual cues and found that both were influenced by experience during early stages of live. Interestingly, the timing of the learning for preferences in the two modalities was different though, with females that had a shorter time available to learn to prefer male features did learn to prefer the olfactory cues, but not the visual cues.

In nature, swordtails live in streams in a mountainous area, where population sizes can be small and highly variable (see picture below of lab sampling and how small the streams can be!). Females may thus have variable opportunities to observe male or female adults of their own species. Why they tune in more to the olfactory cues we can’t explain yet, but given that females are more ‘true to their species’ with olfactory cues than visual cues, this is a very interesting finding.

I think this paper nicely underscores that a closer look at the ontogeny of mate preferences can help explain mate choice preferences, and how they in fact may differ between sensory modalities within a species!

Beyond the Fst-Qst comparison: Insights from the EGRU-blog

You are probably aware of the fact that there are many problems of Fst-Qst-comparisons to infer selection, and this method is also known to have weak statistical power. Essentially, this means that even if selection acts on a phenotypic trait, this method might not be able to detect it, and a finding that Qst equals Fst does not mean that selection is not operating on the trait in question. This low statistical power is a problem, because if one finds a positive result, one can always say that selection has operated on the trait of interest, but not much can be said if one finds a negative result. The trait might then be "neutral" and not subject to selection - or it might be subject to selection, but we cannot detect it with the current method.

There might be solutions and alternatives to the Fst-Qst-comparisons, however. At Juha Merilä's research group blog "EGRU-blog", he refers to a recently published theory-paper in Genetics, which seems like an interesting read. Although I have not read this paper in detail, it is a paper worth keeping in mind, and worth returning to in the future. I took the liberty to borrow the picture from Juha's blog and some of the text where he explains the main implications of their study:

"The main point here to note is that this method allows detection of signatures of selection also in the case where Fst =Qst: the selection in these cases (c,d) is inferred from the fact that population centroids tend to cluster according to selective regime (color) rather than their ancestry (shape of the symbol). It is also worth pointing out that the new method accounts for many other technical problems that have plagued traditional Fst-Qst comparisons. Read the paper and become enlightened!"

To this, I would like to add that it is unlikely that we will ever find the molecular method that can replace the vastly superior method of directly measuring natural or selection in the wild, or quantify quantitative genetic patterns that reveal the action of past selection. Observing something directly, and trying to quantify it, will certainly always reveal more about agents of selection and mechanisms, than indirect inferences like the Fst-Qst comparison.

This does of course not mean that these indirect methods should never be used. Far from it, and we have used such methods in the past in this,  this and this study of ours, for example. But these methods can only be a first step, and if selection is inferred, it should only be considered as a preliminary working hypothesis, that needs to be experimentally corroborated. And moreover, some forms of selection, such as negative frequency-dependent selection, might seldom, or never be detectable when there is weak genetic differentiation between populations (precluding the prospects of finding a pattern where Qst < Fst), and in these cases, direct experimental field studies might be the only possible option. There is never an excuse to avoid going out the field or doing experiments in evolutionary biology, if it is possible.

Annual Systematics-meeting in Lund 21-22 November 2011

You might not yet be aware of this, but on November 21-22 2011, the Annual Systematics-meeting ("Systematikdagarna") will take place at Palaestra in Lund. You can find som useful information here, including some information about invited speakers. The final programme will be out later.

In spite of its name, this meeting has over the last years evolved to become more of an annual Swedish Evolution-meeting, and thus not only systematics sensu strictu. For instance, topics like speciation processes and genetic variation within and between populations are certainly also included under the umbrella "systematics" these days (as they have long been in many other countries than Sweden, where there is a less strict definition of the field). One sign of this broadening of the term systematics is the fact that I, who is primarily a population biologist and evolutionary ecologist, was invited as a plenary speaker in 2008, when the same meeting was held at the Agricultural University of Ultuna, close to Uppsala.

I would therefore encourage you all, especially Anna, Maren and Machteld, to send in an oral contribution or a poster. They seem to prefer spoken contributions in Swedish, but I do not think it is that strict. In any case, all of you have probably talks ready which you have given on other occasions that can readily be modified for the purpose of this meeting. You will also have the chance to reach out to a broad audience of systematists and evolutionary biologists in Sweden. Information about how to pay and sign up can be found here and here.

Lab meeting 22/09/2011 at 1pm on MARINE SPECIATION. Guest: Kendall Clements

Ecological speciation has received a lot of attention in the past decade, and many papers have been published since the appearance of Dolph Schluters 2001 book on adaptive radiations, which stresses the importance of ecology in evolution. Recently, people have criticized that some scientists see evidence for ecological speciation in every system, and some even think that ecological speciation is on its way to become a dogma in itself. But has ecological speciation received the same amount of attention in all systems?

The majority of what is known about patterns and processes of speciation derives from studies on terrestrial and freshwater species, which usually inhabit environments that are geographically heterogeneous. This heterogeneity might account for the importance that some scientists attribute to allopatric speciation in general. Marine organisms, on the other hand, are normally found in environments where geographic barriers and environmental structure are less, and where dispersal is often large. For these reasons, the mechanisms that drive speciation in terrestrial and freshwater taxa may be different from those that act in marine species, and the patterns of speciation may be significantly different. On Friday the 23 of September (1-2pm), Kendall Clements from the University of Auckland, New Zealand, is going to give a talk about parrotfishes and drummers in the context of adaptive radiations, where he is going to argue that ecological speciation has not received enough attention in a marine setting. 

We will have a lab meeting on Thursday the 22 of September, starting at 1pm, to discuss these topics with Kendall. We will read two papers that are both relevant to marine speciation. The first one is the paper by Streelman and Danley (2003), which considers ecological divergence and sexual selection as progressive stages in vertebrate adaptive radiations. The second paper that is interesting in the context of marine speciation is the Van Doorn et al. (2009) paper, which examines the relationship between ecological speciation and sexual selection in a modeling context.

I will bring FIKA and make sure that we have coffee, since Kendall will be jetlagged. 

Hope to see you all there, Maren

New publications on the molecular ecology and population structure of Ischnura elegans

Over the last two years, we have started to look more into the molecular population structure of the blue-tailed damselfly Ischnura elegans, and have tried to relate the molecular structure to ecological patterns and processes. As a result of our efforts, we have recently published a number of papers which we would like to draw your attention to. The first study investigates the large scale molecular and ecological structure of I. elegans populations across Europe. The second paper studies the frequencies of different colour morphs in Ischnura spp. populations across Europe, and investigated the processes that could explain the different patterns among regions. Lastly, the third study examines contemporary hybridisation between the sister species I. elegans and I. graellsii in Europe, and quantifies the effect of introgression on the colour morph frequencies in both species. 

Photograph by Erik Svensson: The blue-tailed damselfly

Below you can find the titles and abstracts of the three papers. 

Wellenreuther, M., R. A. Sánchez-Guillén, A.Cordero-Rivera, E. I. Svensson, and B. Hansson. 2011. Environmental andClimatic Determinants of Molecular Diversity and Genetic Population Structurein a Coenagrionid Damselfly. PLoS ONE 6:e20440.

ABSTRACT: Identifying environmental factors that structure intraspecific genetic diversity is of interest for both habitat preservation and biodiversity conservation. Recent advances in statistical and geographical genetics make it possible to investigate how environmental factors affect geographic organisation and population structure of molecular genetic diversity within species. Here we present a study on a common and wide ranging insect, the blue tailed damselfly Ischnura elegans, which has been the target of many ecological and evolutionary studies. We addressed the following questions: (i) Is the population structure affected by longitudinal or latitudinal gradients?; (ii) Do geographic boundaries limit gene flow?; (iii) Does geographic distance affect connectivity and is there a signature of past bottlenecks?; (iv) Is there evidence of a recent range expansion and (vi) what is the effect of geography and climatic factors on population structure? We found low to moderate genetic sub-structuring between populations (mean F_ST = 0.06, D_est = 0.12), and an effect of longitude, but not latitude, on genetic diversity. No significant effects of geographic boundaries (e.g. water bodies) were found. F_ST-and D_est-values increased with geographic distance; however, there was no evidence for recent bottlenecks. Finally, we did not detect any molecular signatures of range expansions or an effect of geographic suitability, although local precipitation had a strong effect on genetic differentiation. The population structure of this small insect has probably been shaped by ecological factors that are correlated with longitudinal gradients, geographic distances, and local precipitation. The relatively weak global population structure and high degree of genetic variation within populations suggest that I. elegans has high dispersal ability, which is consistent with this species being an effective and early coloniser of new habitats. 

Sánchez-Guillén, R., B.Hansson, M. Wellenreuther, E. I. Svensson, and A. T. Cordero-Rivera. 2011a. Theinfluence of stochastic and selective forces in the population divergence offemale colour polymorphism in damselflies of the genus Ischnura. Heredity.

ABSTRACT: Disentangling the relative importance and potential interactions of selection and genetic drift in driving phenotypic divergence of species is a classical research topic in population genetics and evolutionary biology. Here, we evaluate the role of stochastic and selective forces on population divergence of a colour polymorphism in seven damselfly species of the genus Ischnura, with a particular focus on I. elegans and I. graellsii. Colour-morph frequencies in Spanish I. elegans populations varied greatly, even at a local scale, whereas more similar frequencies were found among populations in eastern Europe. In contrast, I. graellsii and the other five Ischnura species showed little variation in colour-morph frequencies between populations. F_ST-outlier analyses revealed that the colour locus deviated strongly from neutral expectations in Spanish populations of I. elegans, contrasting the pattern found in eastern European populations, and in I. graellsii, where no such discrepancy between morph divergence and neutral divergence could be detected. This suggests that divergent selection has been operating on the colour locus in Spanish populations of I. elegans, whereas processes such as genetic drift, possibly in combination with other forms of selection (such as negative frequency-dependent selection), appear to have been present in other regions, such as eastern Europe. Overall, the results indicate that both selective and stochastic processes operate on these colour polymorphisms, and suggest that the relative importance of factors varies between geographical regions. 


Sánchez-Guillén, R. A., M.Wellenreuther, A. Cordero-Rivera, and B. Hansson. 2011b. Admixture analysisreveals introgression in Ischnura damselflies in a recently establishedsympatric region. BMC Evol. Biol. 11:210.

ABSTRACT: Studying contemporary hybridization increases our understanding of introgression, adaptation and, ultimately, speciation. The sister species Ischnura elegans and I. graellsii (Odonata: Coenagrionidae) are ecologically, morphologically and genetically similar and hybridize. Recently, I. elegans has colonized northern Spain, creating a broad sympatric region with I. graellsii. Here, we review the distribution of both species in Iberia and evaluate the degree of introgression of I. graellsii into I. elegans using six microsatellite markers (442 individuals from 26 populations) and five mitochondrial genes in sympatric and allopatric localities. Furthermore, we quantify the effect of hybridization on the frequencies of the genetically controlled colour polymorphism in females of both species.

Lab-meeting on epigenetic inheritance and evolution

Following the suggestions of Machteld Verzijden and Anna Runemark, I suggest we denote next lab-meeting to discuss epigenetic inheritance and its (possible) evolutionary consequences to epigenetic inheritance. I suggest that we discuss two recent papers, one more theoretical in American Naturalist by Troy Day and Russel Bonduriansky which can be found here, and a review in Nature Reviews Genetics by Danchin et al. which can be found here. I post the Abstract of that paper below.

Please read both these papers, and not in the last minute, as it is a difficult topic, but the more we know in advance, the more enlightened will the discussion be.

Note that next lab-mating will take place in "Argumentet" between 10.00 and 12.00 on Tuesday 6 September 2011. After that, our regular lab-meetings will take place between 10.00 and 12.00 on Thursdays. Fika volunteers are always welcome.

Beyond DNA: integrating inclusive inheritance into an extended theory of evolution
Danchin, E (Danchin, Etienne)1; Charmantier, A (Charmantier, Anne)2; Champagne, FA (Champagne, Frances A.)3; Mesoudi, A (Mesoudi, Alex)4; Pujol, B (Pujol, Benoit)1; Blanchet, S (Blanchet, Simon)1,5
Nature Reviews Genetics 12: 475-486
Abstract: Many biologists are calling for an 'extended evolutionary synthesis' that would 'modernize the modern synthesis' of evolution. Biological information is typically considered as being transmitted across generations by the DNA sequence alone, but accumulating evidence indicates that both genetic and non-genetic inheritance, and the interactions between them, have important effects on evolutionary outcomes. We review the evidence for such effects of epigenetic, ecological and cultural inheritance and parental effects, and outline methods that quantify the relative contributions of genetic and non-genetic heritability to the transmission of phenotypic variation across generations. These issues have implications for diverse areas, from the question of missing heritability in human complex-trait genetics to the basis of major evolutionary transitions.