First lab-meeting 8 January 2013: Evolution of sex differences in canalization and plasticity

Male pheasant (Phasanius colchicus), a sexually very dimorphic bird. 

Photo: Erik Svensson

Posted by Erik Svensson

It is time for the first lab-meeting of 2013, and since it will be my birthday (8 January), I will bring a cake. I want to dedicate this lab-meeting to two papers about sex differences in plasticity and its opposite (canalization). You will find the Abstracts below, and you can download these two papers here and here.

I do also want to take the opportunity to briefly (15-30 minutes) present some ongoing work that I have been doing with Machteld, Maren and Anna Runemark about sex-differences in learned mate preferences and responses to heterospecifics, based on some experiments we have done on male and female banded demoiselles (Calopteryx splendens). This is also related to some of Machtelds ongoing work on the developmental plasticity of preference curves and mate preference learning, which we can also discuss a bit. Hopefully, there will then be a smooth transition between this short presentation and the papers we will discuss.

For the rest of the semester, Machteld Verzijden (machteld.verzijden@biol.lu.se) is responsible for setting up a "Google Docs"-link soon so that we can all sign up for lab-meetings and take the opportunity to arrange at least one lab-meeting during next semester (including picking 1-2 papers and/or prepare a presentation, bring fika, writeup a blog post, post it on the Facebook group).

Details about the lab-meeting next week:

Time: 8 January 2013 at 10.30
Place: "Argumentet", 2nd floor, Ecology Building

Sex Differences in Phenotypic Plasticity Affect Variation in Sexual Size Dimorphism in Insects: From Physiology to Evolution

Annual Review of Entomology

Vol. 55: 227-245 (Volume publication date January 2010)

R. Craig Stillwell, Wolf U. Blanckenhorn, Tiit Teder, Goggy Davidowitz, and Charles W. Fox  
Males and females of nearly all animals differ in their body size, a phenomenon called sexual size dimorphism (SSD). The degree and direction of SSD vary considerably among taxa, including among populations within species. A considerable amount of this variation is due to sex differences in body size plasticity. We examine how variation in these sex differences is generated by exploring sex differences in plasticity in growth rate and development time and the physiological regulation of these differences (e.g., sex differences in regulation by the endocrine system). We explore adaptive hypotheses proposed to explain sex differences in plasticity, including those that predict that plasticity will be lowest for traits under strong selection (adaptive canalization) or greatest for traits under strong directional selection (condition dependence), but few studies have tested these hypotheses. Studies that combine proximate and ultimate mechanisms offer great promise for understanding variation in SSD and sex differences in body size plasticity in insects.

CONTRASTING THEORY WITH THE EMPIRICAL DATA OF SPECIES RECOGNITION

Author(s): Ord, T.J.; King, L, Young, A.R.

Evolution Volume: 65   Issue: 9   Pages: 2572-2591   DOI: 10.1111/j.1558-5646.2011.01319.x   Published: SEP 2011

Abstract: We tested hypotheses on how animals should respond to heterospecifics encountered in the environment. Hypotheses were formulated from models parameterized to emphasize four factors that are expected to influence species discrimination: mating and territorial interactions; sex differences in resource value; environments in which heterospecifics were common or rare; and the type of identity cues available for species recognition. We also considered the role of phylogeny on contemporary responses to heterospecifics. We tested the extent these factors explained variation among taxa in species discrimination using a meta-analysis of three decades of species recognition research. A surprising outcome was the absence of a general predictor of when species discrimination would most likely occur. Instead, species discrimination is dictated by the benefits and costs of responding to a conspecific or heterospecific that are governed by the specific circumstances of a given species. The phylogeny of species recognition provided another unexpected finding: the evolutionary relationships among species predicted whether courting males within species-but not females-would discriminate against heterospecifcs. This implies that species recognition has evolved quite differently in the sexes. Finally, we identify common pitfalls in experimental design that seem to have affected some studies (e.g., poor statistical power) and provide recommendations for future research.

Lab-meeting on the evolution of plasticity in changing environments

This Wednesday (January 11 2012), we will discuss a relatively recent theoretical and conceptual paper in PLoS Biology entitled "Adaptation, plasticity and extinction in a changing environment: towards a predictive theory".  You can download it here.


Although this paper was published as recently as in 2010, but has already received 79 citations - a sign of a quite an influential paper. This is not surprising as it connects such topics as climate change, thermal adaptation and niche modelling with the evolution of phenotypic plasticity - all very important and central topics in ecology and evoutionary biology. Below you will find the Abstract for the paper. One of the co-authors is legendary evolutionary quantitative geneticist Russel Lande, by the way.

Time: Wednesday, January 11, 2012
Place: "Argumentet"

 

Summary 

Many species are experiencing sustained environmental change mainly due to human activities. The unusual rate and extent of anthropogenic alterations of the environment may exceed the capacity of developmental, genetic, and demographic mechanisms that populations have evolved to deal with environmental change. To begin to understand the limits to population persistence, we present a simple evolutionary model for the critical rate of environmental change beyond which a population must decline and go extinct. We use this model to highlight the major determinants of extinction risk in a changing environment, and identify research needs for improved predictions based on projected changes in environmental variables. Two key parameters relating the environment to population biology have not yet received sufficient attention. Phenotypic plasticity, the direct influence of environment on the development of individual phenotypes, is increasingly considered an important component of phenotypic change in the wild and should be incorporated in models of population persistence. Environmental sensitivity of selection, the change in the optimum phenotype with the environment, still crucially needs empirical assessment. We use environmental tolerance curves and other examples of ecological and evolutionary responses to climate change to illustrate how these mechanistic approaches can be developed for predictive purposes.

On intralocus sexual conflict in hermaphroditic animals

Former lab-member Jessica Abbott, who defended her PhD-thesis in Lund in 2006 has a review-paper published in Proc. R. Soc. Lond. B., that can be found here. After finishing her PhD, Jessica moved for a two-year postdoc to Adam Chippindale's lab at Queens University in Canada, and then back to Sweden and Uppsala University (Ted Morrow's lab).

Jessica will visit the Biology Department in Lund on October 14 for a Thursday Seminar in the "Blue Hall" (14.00, Thursday 14 October 2010). One possibility would be to read her review-paper on our lab-meeting that week (Thursday October 13, at 10.15) to prepare for her talk. Here is the abstract of Jessica's article in Proceedings:


Intra-locus sexual conflict and sexually antagonistic genetic variation in hermaphroditic animals

Jessica K. Abbott

Abstract

Intra-locus sexual conflict results when sex-specific selection pressures for a given trait act against the intra-sexual genetic correlation for that trait. It has been found in a wide variety of taxa in both laboratory and natural populations, but the importance of intra-locus sexual conflict and sexually antagonistic genetic variation in hermaphroditic organisms has rarely been considered. This is not so surprising given the conceptual and theoretical association of intra-locus sexual conflict with sexual dimorphism, but there is no a priori reason why intra-locus sexual conflict cannot occur in hermaphroditic organisms as well. Here, I discuss the potential for intra-locus sexual conflict in hermaphroditic animals and review the available evidence for such conflict, and for the existence of sexually antagonistic genetic variation in hermaphrodites. I argue that mutations with asymmetric effects are particularly likely to be important in mediating sexual antagonism in hermaphroditic organisms. Moreover, sexually antagonistic genetic variation is likely to play an important role in inter-individual variation in sex allocation and in transitions to and from gonochorism (separate sexes) in simultaneous hermaphrodites. I also describe how sequential hermaphrodites may experience a unique form of intra-locus sexual conflict via antagonistic pleiotropy. Finally, I conclude with some suggestions for further research.

New lab-publication about intralocus sexual conflict in polymorphic damselflies

Former PhD-student Jessica Abott and I have a forthcoming article ("Early view") in Evolutionary Ecology Research (EER) that might be of interest. It deals with intersexual genetic correlations in different female colour morphs of the damselfly Ischnura elegans, that we have studied intensively in our lab over the last ten years.

These intersexual genetic correlations differ significantly between the different female morphs, the most striking pattern being higher intersexual genetic correlations ("more male-like") in the androchrome (male-mimicking) female morph. The paper can be found here, and the title is "Morph-specific intersexual genetic correlations in an intraspecific mimicry system". Enjoy!

More reflections about quantiative genetics from Norway

I am currently in Oslo (Norway) at "Centre for Ecological Synthesis and Evolutinary Synthesis" (CEES) where I have been visiting theoretical evolutionary biologist Thomas F. Hansen. Also visiting here are evolutionary geneticists David Houle and Gunter P. Wagner. So it has been an interesting group of people to discuss, as you understand.

I talked to David Houle about the paradox that the molecular markers explain only a tiny fraction of total genetic variation in human height (see my previous bloggpost), whereas classical quantitative genetic studies (based on covariances between relatives) indicate that the real amount of genetic variation is substantially higher (between 80 and 90 %). David Houle interpreted this discrepancy very much as I did: it provides support for the so-called "infinitisemal model" in quantitative genetics, as formulated (among others) by Russel Lande.

In other words, many loci, perhaps the vast majority of all coding genes, influence human height, but each has a very small contribution in terms of percentages. This is not surprising as many independent genetic factors are likely to influence "condition" or growth, each giving a very small contribution. This makes the prospects for molecular genetic association studies quite bleach, since this approach can only (because of statistical power issues) only detect those few factors that have a relatively large effect. We are left with a situation where quantitative genetic approaches "capture" more of the existing variation than do molecular association studies that fail to detect all these small genetic factors.

This also means that we should perhaps be aware of the fact that many beatiful genetic association studies and studies of candidate genes such as the melanocortin receptor (MC1R) studied by Hopi Hoekstra's laboratory might be untypical and not representative for the vast majority of quantitative traits governed by many different genes (height being one of them). This is not surprising to me, however, it also shows that there is a lot of interesting work remaining to be done and a lot of theoretical and empirical challenges ahead.

Why molecular genetics will not replace quantiative genetics

Today, at our lab-meeting, I briefly mentioned an interesting bloggpost by Juha Merilä at his research group's blogg, that I would like to discuss a bit. The reason is that it is not only interesting from the viewopoint of quantitative genetics vs. molecular genetics per se, but also of its wider implications in terms of the value of reductionism in science vs. emergent properties of biological systems. What do I mean by this?

Emergent properties of systems simply means that "the whole is more than the sum of the parts". This is nothing metaphysical, but it means that one might not fully understand a system simply by de-composing it in to separate parts, because the parts often interact with each other. One actually needs to understand how the parts work together, and it is here where I see the value of quantitative genetics. Quantitative genetics is focussed on the "units" (=traits) that we as evolutionary biologists are most interested in and which we would like to understand how they evolve. It focuses on these higher-level units, while at the same time ignoring the details (=the particular single genes governing the traits). This might be perceived as a weakness of quantiative genetics, but others would argue that it is a strength. I will not dwell in to this here.

Although none of us would deny that the traits are governed by many different genes, as well as the environment of course, we do still not fully understand the genetic basis of the vast majority of traits, in spite of the explosion of molecular information and the presence of fully-sequenced genomes. And if you ask me, I am not sure we will necessarily get the answers to these fundamental questions in biology simply by sequencing even more, or by hoping that new molecular techniques will solve all the remaining questions. In short: the whole will always be more than the sum of the parts, and quantitative genetics is still live and kicking. At least in some circles.

Back to Juha's bloggpost. An interesting "paradox" is that quantitative genetic studies of human height indicate that heritability of height is very high: between 80 and 90 %. In other words, height is a highly heritable trait that can rapidly evolve by natural or sexual selection. One would therefore think that height would be an excellent trait to focus on if we wish to find candidate genes or do genome-wide association studies to identify the precise genes. Such a study has indeed been performed, but as the blogg "Genetic Future" rather brutally points out, these studies have been "a resounding disappointment".

Some more specific examples of these disappointing results:

The first genome-wide association for height, published in September last year, examined 4,921 individuals and found a single significant and replicable variant associated with height (in the HMGA2 gene) that explained a meagre 0.3% of the variation in the general population. The second such scan, published in January this year, examined 6,669 individuals. This study confirmed the HMGA2 finding and identified one further significant signal, this time near the GDF5 and UQCC genes, which again explained less than 0.5% of the total variation. I saw an abstract at the American Society of Human Genetics meeting last year (as yet unpublished, as far as I can tell) in which a genome scan was reported for 10,737 individuals, which pulled out a total of 8 associated variants which together explain just 3% of the variance in height.

To summarise these results: to date genome-wide scans for height, even extremely well-powered ones with more than 10,000 participants, have identified variants responsible for less than 5% of the variation in this trait - despite height being a trait that is largely genetically determined and varies substantially between humans. What's going on?

Well, I certainly do not know the answer, and neither does Juha or the blogger "Genetic Future". But we can safely conclude that a major fraction of the genetic variation in height is "missing" and not picked up in these genome-wide association studies and by the molecular markers. Hopefully, future studies can improve resolution and increase these depressingly low percentages somewhat. However, these low percentages should be somewhat worrying, at least for those who thought that it would be easy to study the molecular basis of this trait. Especially given that we already know that there is ample genetic variation for human height from the quantitative genetic studies.

It seems to me that either the heritability estimates have been severely inflated (e. g. by maternal effects), or the molecular markers do not fully capture all the genetic variation in human height. Although it is definitely possible that heritability is somewhat overestimated, I doubt that heritability will only be a few percent, as the molecular marker studies indicate. Most morphological traits have heritabilities much higher than a few percent, so it seems a safe conclusion that the molecular markers miss a large amount of the genetic variation that is actually present. Therefore, it seems as if the association studies are missing the big picture. The results from these genome-wide association studies must in any case be a big dissappointment, given the large research resources that have been put in to them and the HUGE sample sizes in these studies.

The EGRU-blogg cites a recent update about this work in Nature, and (musingly?) concludes:

"Read the thought provoking ‘news feature’ from Nature by Brend Maher about the statue puzzle. It might even give some (quantum of?) solace for those sticking with their parent-offspring regressions and tedious experiments while the others in their spotless labcoats are drowning in their high throughput data."

Juha Merilä also comments on another interesting bloggpost with the title "Do we still need quantiative genetics in the 21st Century":

"It seems that people were a bit optimistic about the utility of the new technologies in solving old problems. This has also lead to situation where students have jumped into the fancy wagon of genomics, and left quantitative genetics with some interesting (and unfortunate) consequences of which you can read from here:

http://www3.interscience.wiley.com/cgi-bin/fulltext/119408495/HTMLSTART

Actually, all the 2008 volumes of the Journal of Animal Breeding and genetics feature nice Editorials each which touch some general issues interesting also for Evolutionary Biologists. Go and have a look:

http://www3.interscience.wiley.com/journal/118521919/issueyear?year=2008"

I, myself, is like Juha a big fan of quantitative genetics, and I do of course agree with him and his colleagues that this is a useful tool that is unlikely to be replaced by molecular genetics, neither in the short- nor in the long-term. As a matter of fact, molecular genetics might have its greatest utility as a complement to quantitative genetic approaches, e. g. in the combination of QTL-approaches and estimations of quantitative genetic parameters such as to understand the "anatomy" of genetic correlations. Are genetic correlations mainly a result of linkage disequilibrium or pleiotropy, is one such interesting question that can be adressed by the combination of quantitative genetics and QTL-approaches.

And it might of course always be good to keep in mind that one should be critical of scientific bandwagons and premature claims that new techniques will solve all problems. Finally, do not forget the emergent properties and that the whole is always more than the sum of the parts. Reductionism can be taken too far, particularly in biology.