Journal Of Evolutionary Biology Research Articles

Why and how do Y chromosome stop recombining?

Sex chromosomes either carry a factor like the male-determining factors of mammals (Berta et al., 1990) or the plant Silene latifolia (Westergaard, 1958), or function in balanced sex-determining systems, as in Drosophila (Bridges, 1925) and Caenorhabditis elegans (Meyer, 2022). The sex chromosome pairs of these and several other species include physically extensive fully Y-linked, or male-specific, regions (‘MSY’) that have undergone ‘genetic degeneration’ and lost most of the genes that are carried on the X (X-linked genes are then hemizygous in males). Similar losses of recombination, and similar extensive degeneration, have occurred in the evolution of sex chromosomes in species with female heterogamety, including birds and Lepidoptera, respectively, reviewed by Wang et al. (2014) and Fraisse et al. (2017). The lack of recombination is probably not a direct consequence of carrying the sex-determining genes, or of having an essential role in sex determination, since several unrelated fish have physically small sex-determining regions located within recombining regions (Koyama et al., 2019; Kuhl et al., 2021; Nacif et al., 2022; Reichwald et al., 2015), and the completely sex-linked regions of some plants are smaller than 1 Mb (Akagi et al., 2014; Harkess et al., 2020). These situations can be explained in several ways, for example they could reflect recent evolution of separate sexes, or recent appearance of a sex-determining factor in a genome region in a so-called turnover event reviewed by (Vicoso, 2019). Species whose chromosome pair has undergone changes in which formerly recombining regions stopped recombining with a previously established completely sex-linked region are therefore important, because they tell us that recombination became suppressed after their sex-determining locus evolved. The first case to be discovered was in Eutherian mammals. The earliest enlargement of the MSY involved fusion of the Y with a chromosome, that is an autosome in Marsupials (Waters et al., 2001). This occurred around 115 million years ago (Cortez et al., 2014). Further enlargements caused by subsequent recombination suppression events produced ‘evolutionary strata’ with wide differences in sequence divergence between the Y-X pairs in different regions of the chromosome (Figure 1). Based on the genetic map estimated in females (which probably represents the ancestral order of genes on the added chromosome), divergence stopped most recently near the region that still recombines, the pseudo-autosomal region, or ‘PAR’ (Lahn & Page, 1999; Skaletsky et al., 2003). In the two most recently evolved strata in humans, the median synonymous site divergence values are 14% and 26%, almost as high as for the rest of the added region (Sayres & Makova, 2013). Very varied Y-X divergence, perhaps reflecting strata, is also seen in the plant Silene latifolia, in the carnation family (Bergero et al., 2007; Papadopulos et al., 2015). In the threespine stickleback, whose sex chromosomes evolved without fusions with any autosomes, Y-X divergence shows clear strata like the two in Figure 1b (Peichel et al., 2020), and strata have also been inferred in the ZW pair in Neognathous birds (Wang et al., 2014). A lack of recombination between sex chromosomes may not always reflect such suppressed recombination (Charlesworth, 2019). However, cases when recombination suppression has evolved (shrinking the PAR and changing its boundary with the completely sex-linked region) demand explanation. Several hypotheses have been proposed. One idea is that sexually antagonistic polymorphisms can become established in the PAR (e.g. a male-benefit allele that would reduce fitness in females is more likely to spread if closely linked to the MSY than one with the same fitness effects that is autosomal). Should such a mutation establish a polymorphism, this generates selection for closer linkage with the MSY (Rice, 1987). This idea is difficult to test because, if a non-recombining stratum has evolved, the mutation will be present only in the fully Y-linked region, making genetic analysis impossible. Although such male-benefit mutations might be detectable from expression differences between the sexes at the genes involved (perhaps higher in males), genetic degeneration is expected eventually to reduce expression of Y-linked genes in old evolutionary strata. Another approach is to test for population genomic evidence of balanced polymorphisms that show associations between the alleles and the sex-determining alleles (Dagilis et al., 2022; Qiu et al., 2013). However, if such a signal is found in partially sex-linked region, it still does not tell us whether selection will in the future lead to the evolution of suppressed recombination. Another approach is to search for alternatives that could also explain the evolution of suppressed recombination and ask if they can be ruled out. As described below, some new ideas have recently been proposed. Testing the predictions of these new hypotheses (Figure 2 below) requires studies of newly evolving strata of completely sex-linked genes, and of the PAR boundary regions of genomes, and such studies are becoming possible, using a combination of genome sequencing and genetic mapping. A new study of Silene latifolia and S. dioica (closely related species that hybridize in nature and have homologous XY sex chromosomes), recently published in Journal of Evolutionary Biology (Filatov, 2022), examines such a newly evolved stratum. Y- and X-linked alleles can nevertheless be ascertained by identifying male-specific variants in gene sequences, using samples of males and females from natural populations. This approach allowed the Y-X sequence divergence analyses mentioned above that showed that recombination in parts of the S. latifolia Y chromosome pair became suppressed after the establishment of its male-determining factor. Clear step changes like those in Figure 1 are not seen, and the numbers of genes in the PAR and the MSY strata are unknown, since these species' genomes are as large as the human genome and have not yet been assembled. However, genetic mapping does not suggest an extremely high recombination rate in the S. latifolia PAR, which may thus differ from mammalian PARs, with crossover events concentrated in physically very small regions (Rouyer et al., 1986). Some genes have male-specific variants in S. latifolia, but not in S. dioica, suggesting that S. latifolia has evolved a new stratum of completely sex-linked genes (and a smaller PAR than S. dioica; Campos et al., 2016). The new study ascertained more genes from the recombining end of the S. latifolia X chromosome genetic map and studied them in detail. 22 were fully sex-linked in both Silene species studied (they had male-specific variants in samples from natural populations), and 20 were classified as PAR genes in both species, but 15 PAR genes in S. dioica appear to be fully sex-linked in S. latifolia, forming a young stratum (much younger than the youngest ones in humans described above) suitable for testing ideas about recombination suppression. One recent idea is that a completely sex-linked region (MSY) might gradually expand as sequence divergence near a sex-determining locus or PAR boundary with the MSY hinders pairing of very closely linked sequences in meiosis (Jeffries et al., 2021). MSY-X sequence divergence should then increase with distance from the PAR boundary into the MSY region (Figure 2). A slight trend is seen for Y-X synonymous site divergence in the new S. latifolia stratum, but divergence from the outgroup species S. vulgaris also increases (Filatov, 2022), so mutation rate differences may be responsible (HKA tests, which correct for this effect, detected elevated diversity in PAR genes suggests that the present PAR might have a higher mutation rate than the completely sex-linked regions). Interestingly, Y-X divergence increases sharply between the S. latifolia-specific MSY region and that shared with S. dioica, without any such change in divergence from the outgroup species, suggesting a possibly discontinuous change between strata, as in Figure 1b. The small divergence time between S. latifolia and S. dioica also makes it seem unlikely that loss of pairing could have produced an expansion across a region that includes at least 15 genes (probably at least 500 kb, as the gene density on the S. latifolia X is estimated to be 34 genes/Mb). The threespine stickleback XY pair includes a stratum with slightly higher synonymous site divergence (Ks), but still only 3% or 4%, and more than 500 X-linked genes (Peichel et al., 2020). Again Ks does not increase near the boundary with the older stratum, as predicted. The same is true in the plant papaya, in which divergence is high near the PAR boundary (Wang et al., 2012), consistent with a chromosomal inversion (Figure 1). The other models propose MSY expansions involving chance spread of inversions that prevent recombination between a set of PAR genes and the MSY. This requires an advantage that can outweigh any fertility disadvantages in inversion heterozygotes, including production of gametes with duplications or deficiencies when crossovers occur in paired regions of large inversions. One version (Jay et al., 2022; Olito et al., 2022) proposes that linkage to the male-determining factor prevents new deleterious mutations becoming homozygous in males. This effect is strongest for mutations with large and highly recessive deleterious effects. Accumulation of mutations after the inversion arises can prevent the inversion from fixing in this population, so it must rapidly replace the ancestral Y chromosome population (initially with the X arrangement). The process therefore works best in small populations, and it is not clear whether it can account for observations on the time-course of recombination suppression and evolutionary strata formation. As small inversions are most likely to be involved, such data may not distinguish this process from the previous one—both predict that Y-X divergence within the MSY will increase gradually with distance from the current PAR boundary. Only a few examples of inversions coinciding with evolutionary stratum boundaries have so far been discovered. The two recent strata in humans probably involved inversions, and the others may have done (Lemaitre et al., 2009). In both cases, only a few genes became fully sex-linked (10 genes in stratum IV and seven in the younger stratum V), suggesting that new stratum formation does not require large numbers of genes. Another case (involving 16 genes) was detected in papaya (Wang et al., 2012). Clearly, more detailed studies of such regions will be helpful. However, rearrangements, including inversions, can accumulate after recombination stops in a genome region (Charlesworth et al., 1994), and were detected within human strata (Lemaitre et al., 2009). The third model proposes that alleles that become Y-linked rapidly decrease in expression, in a dosage compensation process that simultaneously increases their X-linked alleles' expression, even before major deterioration of the coding regions of Y-linked genes. This can prevent inversions reverting to the standard arrangement (Lenormand & Roze, 2022). Female-biased expression was indeed observed in the new S. latifolia stratum (Filatov, 2022), perhaps reflecting the assumed decreased expression of Y-linked alleles, while expression of X-linked ones has not yet increased enough to restore expression in males. This model predicts that female expression bias should quickly decrease after sex-linkage evolves. Because dosage compensation evolves as part of the process, strongly female-biased expression should be seen near the boundary of the new stratum with the PAR, but expression of many genes in new (and older) strata should be similar in both sexes. However, the bias in S. latifolia appears to change in the opposite way in the new stratum, increasing to reach the same level as that of genes that are fully sex-linked in both species (in which females have almost double the level in males, a significant difference from PAR genes, which, as expected, show little bias). The bias in the older stratum is consistent with genetic degeneration after recombination had stopped (reviewed in Bachtrog, 2008). Genes with changes that have not yet been fully compensated by evolving higher expression of the X-linked alleles in males will show female-biased expression, as observed in S. latifolia, in which dosage compensation seems to be incomplete (e.g. Papadopulos et al., 2015). It is interesting that degeneration may already have begun in the new stratum genes studied, which have Y-linked alleles as well as X-linked ones, and Y-X sequence divergence of only a few percent. Under the sexually antagonistic polymorphism hypothesis outlined above, one might expect expression differences between the sexes at partially sex-linked gene(s) involved (perhaps often higher in males, the opposite of the pattern predicted by the model just described), while genetic degeneration should reduce expression of most Y-linked genes. Overall, S. latifolia sex chromosome evolution appears to be most likely to be explained by this model, since the other models do not fit the observations. Filatov's new and larger data set also supports previous studies suggesting elevated diversity of PAR genes (using HKA tests, which correct for mutation rate differences), so the present PAR may include sexually antagonistic variants. Whether or not these conclusions will be confirmed once a genome assembly becomes available, this study is valuable for suggesting how an integrated set of increasingly accessible kinds of data may allow empirical tests of the different models in this, and potentially other species with young strata. For instance, in the threespine stickleback, gene expression has been compared between the sexes in somatic tissues, and sex-linked genes were over-represented among biased genes. 155 genes were in the older XY stratum and 47 in the younger one, but the study did not test for a relationship with the genes' positions in the younger stratum (Kitano et al., 2020). The peer review history for this article is available at https://publons.com/publon/10.1111/jeb.14137. This is a commentary and there are no data.

Yes, correct context is indeed the key: An answer to Haave-Audet et al. 2019.

We published a study recently testing the link between brain size and behavioural plasticity using brain size selected guppy (Poecilia reticulata) lines (2019, Journal of Evolutionary Biology, 32, 218-226). Only large-brained fish showed habituation to a new, but actually harmless environment perceived as risky, by increasing movement activity over the 20-day observation period. We concluded that "Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level". In a commentary published in the same journal, Haave-Audet et al. challenged the main message of our study, stating that (a) relative brain size is not a suitable proxy for cognitive ability and (b) habituation measured by us is likely not adaptive and costly. In our response, we first show that a decade's work has proven repeatedly that relative brain size is indeed positively linked to cognitive performance in our model system. Second, we discuss how switching from stressed to unstressed behaviour in stressful situations without real risk is likely adaptive. Finally, we point out that the main cost of behavioural plasticity in our case is the development and maintenance of the neural system needed for information processing, and not the expression of plasticity. We hope that our discussion with Haave-Audet et al. helps clarifying some central issues in this emerging research field.

An association between women's physical attractiveness and the length of their reproductive career in a prospectively longitudinal nationally representative sample.

Why is physical attractiveness more important for women's mate value in long-term mating than in short-term mating? This article replicates Bovet et al.'s (Journal of Evolutionary Biology. 2018; 31:229-238) recent finding that physically attractive women have a later expected age of menopause. I analyzed the prospectively longitudinal, nationally representative sample of women in the National Child Development Study, applying t-test and multiple regression analyses. Analyses showed that girls rated physically attractive at age 7 underwent menarche 3.12 months earlier than other girls, and they had 32% smaller odds of having undergone menopause before age 51. The results suggest that more physically attractive women have longer reproductive careers, explaining why physical attractiveness may be a more important determinant of women's mate value in long-term mating than in short-term mating. Women's physical attractiveness predicts the timing of menarche and menopause, thereby the length of their reproductive careers.

Gender differences in authorships are not associated with publication bias in an evolutionary journal.

The loss of talented women from senior academic positions has partly resulted from a lower number of published papers and the accompanying reduced visibility of female compared to male scientists. The reasons for these gender-differences in authorship is unclear. One potential reason is a bias in the editorial and review process of scientific journals. We investigated whether patterns of authorship and editorial outcome were biased according to gender and geographic location in the Journal of Evolutionary Biology. Such potential bias may contribute to inequality in the field. We found patterns of gender differences in authorship, but this was unrelated to the editorial decision of whether to publish the manuscript. Female first-authors (the lead role) were six times less likely to be named as the corresponding author than male first-authors, and female first-authors were more likely to be displaced as corresponding authors by female co-authors than were male first-authors. We found an under-representation of female first- and last-authors compared to baseline populations of members of the European Society for Evolutionary Biology (which publishes the Journal of Evolutionary Biology) and of Evolutionary Biology faculty at the world top-10 universities for the Life Sciences. Also, manuscripts from Asia were five times more likely to be rejected on the final decision, independent of gender. Overall our results suggest that the peer review processes we investigated at the Journal of Evolutionary Biology are predominately gender-neutral, but not neutral to geographic location. Editorial gender-bias is thus unlikely to be a contributing factor to differences in authorship in this journal.

Retracted: The evolutionary history of colour polymorphism in Ischnura damselflies.

The above article from Journal of Evolutionary Biology, published online on 24 May 2018 in Wiley Online Library (http://wileyonlinelibrary.com), has been retracted on the request of the authors and with the agreement of the Journal's Editor in Chief Wolf Blanckenhorn and John Wiley & Sons, following disagreement on potential corrections to the article after publication. The decision to retract followed significant issues with the methods and analyses of the manuscript that were originally not uncovered during peer-review, but which were subsequently brought to the Journal's attention following publication of the Article on Early View. [Correction added on 2 July 2021, after first online publication: retraction statement has been modified.].

Proceedings B 2015: the year in review

It hardly seems possible that a year has passed since I sat down to write my first editorial as the incoming Editor-in-Chief of Proceedings B, replacing Michael Hassell. The first year has been challenging, as I have learned how to address numerous issues that required expeditious but sound decision-making. The academic publishing world is evolving rapidly and at Proceedings B we strive to keep pace with the changes around us and understand how they might influence our core mission as the flagship biological research journal of the Royal Society. These efforts are well rewarded and truly a privilege because of the endless stream of high-quality submissions encompassing an enormous breadth of subject material. Research in organismal biology has diversified greatly over the past decade and the wide range of articles that we now publish is one of the most impressive features of our journal. I am pleased to report that the journal has gone from strength to strength during 2015. The time to first decision has dropped considerably over the course of the year, and the mean time to first decision over the last six months was just 31.5 days. This reinforces Proceedings B's well-deserved reputation for undertaking rapid and efficient peer review while maintaining high editorial standards. In addition, the number of days from receipt to final acceptance has dropped throughout the year and the mean time to final acceptance over the last six months was just 71 days. This is particularly striking given the very large number of new submissions that we receive, which is on track to be around 3000 for 2015. Citation metrics for Proceedings B remain strong and the journal currently has an impact factor of 5.05 (placing it 8th in the Journal Citation Reports category for Biology), an h-index of 171 and a Source Normalized Impact per Paper value of 1.50. Over the past year, there have been a number of changes at Proceedings B, and we believe these improvements will further increase the attractiveness of the journal to our authors and readers. One important change implemented early in the year, after considerable consultation among the editors, involved rewording the Aims and Scope of the journal on our website. This change reflects, in part, our concern about the submission of articles that were too specialized and focused on single organismal groups, particularly humans. While we still encourage submissions concerned with novel investigations of our species, articles focusing exclusively on humans will only be considered where they have clear relevance to fundamental biological principles and processes, or to other groups of organisms. I hope that the updated Aims and Scope will provide authors with greater clarity regarding the scientific remit of the journal, and the requirements for publication. Proceedings B remains a biology journal, and the new wording reinforces our policy to publish articles that are broadly relevant across all areas of biology. Another significant development at Proceedings B was the initiation of a trial integration with Publons—a web-based platform allowing reviewers to voluntarily obtain credit for reviews undertaken across different journals. By integrating the journal with Publons, we have enabled reviewers to add verified reviews to their profiles more efficiently and therefore receive credit quickly and easily. This has been implemented in response to increasing concerns about ‘reviewer fatigue’ and a growing demand for increased reviewer recognition, including an acknowledgement of the ongoing contributions that reviewers make to scientific journals. I hope that our reviewers will consider taking full advantage of this integration and use it to receive appropriate credit for providing this crucial service to the scientific community. As in previous years, the journal continued with the tradition of publishing review articles of general interest to our readers on topical and often controversial fields. I would like to take this opportunity to encourage potential authors who wish to write interesting, broad reviews to submit proposals to the Reviews Editor, Per Lundberg, via the Editorial office (gro.yteicoslayor@bsgnideecorp). Reviews in Proceedings B must be synthetic in nature and provide new perspectives on a particular field, rather than simply providing summaries of a specific topic. We particularly encourage reviews that provide novel analyses of existing published data. Several stimulating reviews were published in 2015 including the annual Darwin Review, which this year involved an extended evolutionary synthesis by Kevin Laland et al. [1], and the CSEE (Canadian Society for Ecology and Evolution) Review for 2015 [2] in which CSEE past president Jeffrey Hutchings discussed thresholds for impaired species recovery in conservation biology. The 2015 Proceedings B Special Feature published at the end of the year was on Evolution and genetics in medicine, guest edited by Roy Anderson and Brian Spratt. It featured six articles on this emerging and fascinating topic. The Special Feature rounds off a year of celebrations at the Royal Society marking the 350th year since the launch of Philosophical Transactions, which was the first scientific journal in existence and one of the earliest to undertake formal peer review. Another exciting initiative during 2015 was the inaugural Royal Society Publishing photography competition run jointly between Proceedings B and Biology Letters. The competition was a great success receiving over 1000 entries across three categories: Behaviour, Ecology and Environmental Science, and Evolutionary Biology. The winners were announced in November and their images showcased at an event at the Royal Society in London. In August, I was invited to participate in the workshop ‘Meet the Editors’ at the European Society for Evolutionary Biology conference at Lausanne, Switzerland along with editors of other mainstream journals, including Nature, Science, PLoS Biology, Molecular Ecology and Journal of Evolutionary Biology. This event proved to be a very interesting and rewarding experience, with a broad range of topics being discussed based on questions from an audience of several hundred attendees. Of particular note were discussions concerning author appeals of rejections and their drain on editors' time, the pros and cons of double blind reviews, the problems and potential solutions for reviewer fatigue, and ways to ensure balanced gender representation on the Editorial Boards of journals. On this latter issue, I have been working with journal staff at Proceedings B to ensure that our editorial board is more representative of our community of scientists. The journal's board for 2016 includes 28% women—which is higher than in previous years—and a key priority over the next few years will be to increase this proportion. Perusal of the long list on our website of over 100 members of the Editorial Board of Proceedings B never fails to impress me. These dedicated individuals from all over the world form the intellectual backbone of our journal and represent an impressive range of disciplines, experience and academic expertise. Proceedings B could not provide the high-quality and rapid peer review expected by our authors without their support. I therefore take this opportunity to thank all members of the Editorial Board for their hard work on the journal's behalf, particularly those whose terms have recently ended and have now retired from the journal. Similarly, I would like to welcome all the new Associate Editors to the board—we have recruited 15 new Associate Editors over the past few months—and I am looking forward to working with you all over the next few years. I am also pleased to welcome back one of our previous Associate Editors, Loeske Kruuk, who specializes in evolutionary ecology and quantitative genetics, and has recently moved from Edinburgh University to the Australian National University. We are delighted that Loeske has agreed to return to the journal to increase our team of senior editors to seven and her return will strengthen our expertise in the genetics and ecology of wild populations. In closing, I would like to thank all the hard working Editorial Office staff in the London office—Jennifer Kren, Matthew Allinson and Buchi Okereafor—who ensure that the processing and distribution of hundreds of manuscripts each month goes smoothly, and that authors, reviewers and editors receive information in a timely and courteous manner. I am particularly grateful to Rhiannon Meaden, Publishing Editor of Proceedings B, for taking a leadership role in the day-to-day running of the journal over the past year. Rhiannon has been an invaluable source of advice in helping me through my first year and has willingly provided data and information that have helped me to make the numerous decisions that are required as Editor-in-Chief. Given that 2015 was also her first year in the job this has been especially impressive. I am confident that 2016 will be another outstanding year for Proceedings B, and I would be happy to hear from our readership concerning any issues that might improve the services that we provide and particularly the quality of our journal.

Hybridization is important in evolution, but is speciation?

Few contributions have influenced the field of evolutionary biology more than Ernst Mayr’s authoritative book entitled Systematics and The Origin of Species (Mayr, 1942). Here, the author went further than his forerunners in depicting the living world as consisting of discrete clusters of reproductively isolated entities called species and evolutionary differentiation as occurring essentially through a series of speciation events in geographical isolation. Gene flow and hybridization were seen as mainly destructive forces with little evolutionary consequence except in counteracting or retarding evolutionary divergence. Ernst Mayr’s ideas imply that speciation, the process in which populations become reproductively isolated from each other, is the key event in evolutionary diversification. Only when gene flow is brought to a halt are organisms free to diverge unhindered. In the current issue of Journal of Evolutionary Biology, Abbott et al. (2013) tell a very different story. During the ongoing genetic and genomic revolution, students of speciation have come to learn that Mayr’s view is at best incomplete. Hybridization between genetically differentiated populations is widespread, common and has evolutionary consequences. In many circumstances, hybridization plays an integral part in the diversification process and may significantly enhance differentiation. Abbott et al. (2013) present an impressive series of arguments and references to recent empirical and theoretical results on the importance of hybridization in evolution. I wonder, however, whether Mayr’s intellectual universe still affects our interpretations of results and our way of thinking. Can we any longer take for granted that speciation, the final cut-off of gene flow between differentiated taxa, really is this key event in evolution? Could it be that by focusing on speciation as the goal of population divergence or at least as a most significant milestone, we fail to appreciate the full array of processes that result directly or indirectly from hybridization and the consequences these have on diversification and biological organization? My intention here is not to debate species concepts or to question whether species are real. Biodiversity is certainly not a blur of endless forms. Phenotypes are organized into recognizable, relatively discrete clusters, and the evidence is overwhelming that reproductive barriers are important in structuring biodiversity (see e.g. Coyne & Orr, 2004). My intention is rather to focus on the process of evolutionary diversification with an open mind. A great deal of diversification occurs prior to the final completion of reproductive isolation, and as Abbott et al. (2013) point out, some 10–30% of our animal and plant species are known to hybridize and exchange genes with others on a regular basis. A further large proportion of our extant nonhybridizing species (being geographically or reproductively isolated from their closest living relatives at present) are likely to have hybridized some time in the past, even repeatedly. Hence, understanding the evolutionary effects of all this hybridization and gene exchange is utterly important. Also, it is important to investigate the consequences speciation (the final sealing of gene exchange) actually has on the diversification process and in structuring biodiversity. One possible outcome of hybridization is that the introgression of selectively favoured alleles from one population into the other can bring together new adaptive combination of alleles that increase diversification. Abbott et al. (2013) make a five-point argument for why hybridization may enhance adaptive differentiation. In short, they argue that hybridization may act as a possibly more abundant source of adaptive genetic variation than mutation because mutations are rare and hybridization common. They cite Grant & Grant (1994) who estimated that the amount of new, additive genetic variance introduced by hybridization was two to three orders of magnitude higher than that introduced by mutation in Darwin’s finches. We may add one more difference between a mutated allele and one introduced by hybridization. The mutated allele has been altered randomly, whereas the one introduced by hybridization has been shaped by natural selection, albeit in a differentiated genome (deleterious mutations have been purged and any beneficial mutations gone to fixation by selection). Intuitively, I would therefore think that an allele introduced by hybridization on average is more likely to do something good for the organism it enters than a mutated one. The relative distribution of fitness effects of mutated versus introgressed alleles is an interesting empirical question that should be investigated further. Moreover, not only single alleles, but co-adapted suites of interacting genes could potentially be transferred through introgressive hybridization, leading to rapid origin of complex adaptations and evolutionary novelties. Introgression as a source of new genetic variation is by definition not available for completely reproductively isolated species. Hence, if in the long run hybridization and Correspondence: Glenn-Peter Saetre, Department of Biology, Centre for Ecological and Evolutionary Synthesis (CEES), PO Box 1066 Blindern, N-0316 Oslo, Norway. Tel.: +47 22857291; fax: +47 22854001; e-mail: g.p.satre@bio.uio.no

Cichlid Evolution: Lessons in Diversification 2012

This is the second special issue on cichlid evolution hosted by the International Journal of Evolutionary Biology. Once more, we are overwhelmed by the vivid responses to our call for contributions, and thank the authors for their great work. The thirteen papers in this issue, including two reviews, span geographically from Africa to South America and address a wide variety of evolutionary topics including speciation and hybridization, phenotype evolution, and reproductive behaviour. Papers are summarized below in the order in which they appear in this special issue.

Biased Sex Ratios in Plants: Theory and Trends

This paper examines the history of sex ratio theory and the effects of multiple variables on individual and population sex ratios. It also provides examples where plants have been used to test major predictions of sex ratio theory. Then, using over 200 studies from the literature, dioecious plant species are categorized based on their life form, pollination agent, fruit dispersal agent, and sex ratio. A loglinear analysis is used to look at possible correlations between the sex ratio of a population and other life history characteristics. These data are used to examine the predictions made by De Jong et al. (Journal of Evolutionary Biology 15:7, 2002), that relative pollen and seed dispersal distances can be used to predict sex ratio bias. Despite the limited sample size, strong relationships are still observed. 93% of insect pollinated dioecious vines that have biotically dispersed fruit have male-biased sex ratios. Conversely, 61% of shrubs that are wind pollinated and have abiotic fruit dispersal have female-biased sex ratios.

Oxidative stress and the effect of parasites on a carotenoid-based ornament

It has been drawn to our attention that Fig. 1A,C,D in J. Exp. Biol.213, 400-407 appears to show the same data as fig 1a,d,e in a paper published by (some of) the same authors in Journal of Evolutionary Biology (Mougeot et al., 2010). The authors wish to clarify the relationship between these two papers and rectify the lack of cross-referencing.Both papers focus on red grouse and are outputs from the same large-scale field manipulation undertaken in 2006. They represent two, very different, stand-alone studies addressing different conceptual issues. The central experimental manipulation of both papers is the drug treatment of birds. The authors felt it was necessary to include background data in each paper to give the reader confidence in the efficacy of the experimental treatment and to allow the reader to better understand and interpret the main results of the papers, which explore very different physiological mechanisms that influence ornamental colouration.For this reason, the treatment effects on parasite burden and comb colouration were presented in both papers, although a different index of comb redness was used [adjusted R-values (fig. 1e in J. Evol. Biol.) vs adjusted R/(G+B) values (Fig. 1C in J. Exp. Biol.)]. Both indices are accurate reflections of comb redness, gave similar results and have been used in previous studies in different contexts to characterize comb colour. Both papers also include the same data on levels of circulating carotenoids [Fig. 1D in J. Exp. Biol.; fig. 1d in J. Evol. Biol.]. The authors feel the inclusion of these data in both papers can be justified conceptually. In the J. Exp. Biol. paper, the trade-off between the use of carotenoids for colouring ornaments vs dealing with oxidative stress is central to the key question. In the J. Evol. Biol. paper, these data reinforce the argument that carotenoid levels and ornamental colouration covary with corticosterone levels.The reiteration of background data on parasite removal and carotenoid levels does not compromise the uniqueness of each paper. The papers were submitted to, and published by, the respective journals in parallel, and the absence of cross-referencing was an oversight on the part of the authors, who acknowledge that the figure legends should have cited the corresponding paper and that the different indices used for comb redness should have been clarified.Consequently, the text of Fig. 1 in the J. Exp. Biol. paper should have read:Fig. 1. Mean ± s.e.m. changes over time in (A) T. tenuis abundance (worms male−1) (reproduced from Mougeot et al., 2010); (B) comb area (mm2); (C) comb redness (adjusted R/(G+B)-value; see Materials and methods) (data from Mougeot et al., 2010); (D) plasma carotenoid concentration (mg ml−1) (reproduced from Mougeot et al., 2010); (E) plasma concentration of malondialdehyde (MDA; nmol ml−1) and (F) plasma TAS (total antioxidant status; mmol ml−1). White squares: control males; black squares: treated (dosed) males (purged of parasites). Numbers above error bars refer to sample size (number of males).The following reference should also have been included in the Reference list:Mougeot, F., Martinez-Padilla, J., Bortolotti, G. R., Webster, L. M. I. and Piertney, S. B. (2010). Physiological stress links parasites to carotenoid-based colour signals. J. Evol. Biol.23, 643-650.The authors apologise for any inconvenience caused.

How the European Society for Evolutionary Biology and the Journal of Evolutionary Biology were founded

How the European Society for Evolutionary Biology and the <i>Journal of Evolutionary Biology</i> were founded

Social semantics: toward a genuine pluralism in the study of social behaviour

Pluralism is the coexistence of equivalent theoretical frameworks, either because they are historically entrenched or because they achieve separate insights by viewing the same process in different ways. A recent article by West et al. [Journal of Evolutionary Biology (2007) vol. 20, 415-432] attempts to classify the many equivalent frameworks that have been developed to study the evolution of social behaviour. This article addresses shortcomings in the West et al.'s article, especially with respect to multilevel selection, in a common effort to maximize the benefits of pluralism while minimizing the semantic costs.

Convergence of metabolic rate of cultured cells from animals of different sizes

APPETITE, OBESITY, DIGESTION, AND METABOLISMConvergence of metabolic rate of cultured cells from animals of different sizesDenys N. WheatleyDenys N. WheatleyPublished Online:01 Jun 2007https://doi.org/10.1152/ajpregu.00102.2007This is the final version - click for previous versionMoreSectionsPDF (37 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat cultured fibroblasts of cell lines from animals of different size have similar activities for a range of different enzymes and metabolic rates that converge on the similar values despite the metabolic rates of the animals of different sizes having quite distinctly different basal metabolic rates (BMRs). In discussing this “normalization,” the data support experimentally a previous hypothesis based on circumstantial evidence. However, the experimental plan and the cell type chosen for analysis do not provide the best evidence to confirm this hypothesis.In mammals (homeotherms), it is thought that a general allometric relationship exists between metabolic rate and body mass. While this is not usually disputed as a rule of thumb, some groups have argued persistently that the relationship is more precise than others would maintain. The formula proposed is that BMR is proportional to M3/4 (14). It would be surprising to find these formulae applied across the board in mammals, and equally surprising of West and Brown (13) to consider that many deviations would not undermine this relationship. Where exceptions are numerous, any hypothesis is inevitably weakened. Unless one can explain exceptions to the alleged “norm,” the general relationship cannot be regarded as a “mathematical law” of which, incidentally, there are none in biology. The problem of the range within any species also needs to be mentioned (8).Proposed Basis of the Relationship Between Body Mass and Metabolic RateSmall mammals have high mass-specific BMRs, whereas large mammals have much lower BMRs. Although measurement of BMR is not straightforward, this general rule has been known for decades. Small mammals lose heat rapidly because their surface area-to-body mass ratio is high, whereas it decreases in large animals as mass increases. This gives a 2/3 rather than a 3/4 power law, and does not take into account that some animals might be better insulated than others (e.g., the arctic fox). Thus, the BMR of a man will vary depending on whether he is clothed or naked. Since we are talking about whole organisms (typically mammals), it is reasonable to assume that the heat produced by metabolic activity will be the normalized sum of that produced by the cells from every organ and tissue of the body (10, 12), e.g., liver cells have much higher metabolic throughputs than connective tissue. West et al. (14), however, attribute the allegedly universal 3/4 power scaling not to the different contributions of different organs nor to the surface-to-volume ratios in animals of different body mass, but to the fractal geometry of resource supply networks, which they consider to be a biologically universal.What Sets the Metabolic Rates in Different Tissue and Different Species?In this issue of American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Brown et al. (2) proclaim in the title that “Metabolic rate does not scale with body mass in cultured mammalian cells,” which will in literal terms not be self-evident to general readers. But the underlying question in it is: What sets the metabolic rates in different tissues and animals? The premise underlying much of the discussion of this problem is that some intrinsic regulatory mechanism is involved. Any such regulatory mechanism would have to operate down to the cellular and molecular levels; but what sort of control could possibly regulate general metabolic activity? No one has a compelling answer (1).Role of the MitochondrionThe organelle that clearly demands attention is the mitochondrion. In general, heat production by a homeotherm maintains the body temperature at ∼37°C, although a lot may be insensibly lost. When extra heat is required, mitochondria can become increasingly uncoupled. Porter and Brand (11) showed that freshly-isolated mitochondria from horse liver metabolize 10 times slower than from mice liver, and on three accounts they explained why this was so. Their findings corroborate the work of Krebs (9), who found significant differences in the metabolic activity of freshly isolated liver slices from animals of considerably different masses, supporting the notion of intrinsic differences among cells (tissues) from different species. Different enzyme affinities, different membrane transporter densities, levels of cofactors, etc., will all contribute to these “intrinsic differences.”Metabolic Activity in Cultured CellsReturning to cells placed in culture, one might expect that these differences would level out in time in a standardized medium, and therefore cells from different species would converge toward similar metabolic activities. This argument was promulgated by Wheatley and Clegg (16), backed up by evidence presented in Clegg and Wheatley (3), and supporting Coulson's (5) beautifully clear exposition on the importance of delivery rates of metabolites in animals of different sizes. Coulson (4) made another simple point, that once a substrate has entered the cell, the intracellular enzymes have little choice but to act on it. If we knew more about the delivery rates of substrates to cells in situ in different-sized animals, we may well find a scaling formula that is much more relevant and reasonable. In principle, this affords some justification for the “resource supply network” approach taken by West et al. (15).An Experimental Attempt to Prove the HypothesisIn Brown et al. (2), the crucial issue was to carry out experiments that establish whether or not a scaling factor is retained in recently isolated homologous cells (cell “lines”) from small and large animals. Unfortunately, Brown's group did not use primary cultures. Even if they had, it would have taken quite a number of generations to obtain sufficient cells for their analyses. The choice of fibroblasts was also unfortunate because dermal fibroblasts in vivo are quite inactive, with very low metabolic activity. Their activity will rise in culture, so cells from different species might all have risen to similar levels simply by placing them in the same rich medium (as expected on Coulson's principle). Relevant details are also missing on the American Type Culture Collection (Manassas, VA)-acquired “cell lines”, and we are not told much about how long the cultures were incubated before being analyzed. However, the fact that the enzymes chosen for study all had similar activities suggests the normalization of activity would not be unexpected.In conclusion, the outcome of the study is nevertheless incontrovertible, that any scaling that might have existed in vivo from different species is lost when the cells are cultured, as already predicted (2, 16). Examination of metabolic changes during culturing of cells that become normalized is now a crucial requirement, and the obverse experiment (setting out cells of high activity in vivo in culture) would be more relevant.An Alternative HypothesisWhereas the West et al. (14) model predicts that (metabolically active) cells will lose their in situ scaling characteristics when they are grown in culture, the quantum metabolism theory of Demetrius (6, 7) predicts the opposite. Quantum metabolism attempts to infer whole organism metabolic rates from the metabolic activities of component cells. Based on chemiosmotic energy transduction, a concept of energy storage in membrane biomolecules and the perception that these energy storage levels are in principle quantized, the argument for the theory is developed using the same mathematical formalism as the quantum theory of solids. This theory makes a number of predictions that are critically testable by experiment, of which the retention of scaling by appropriately cultured cells is one. It is therefore particularly unfortunate that the experiments of Brown et al. (2) were conducted in a manner that failed to provide either compelling corroboration or refutation of either the West et al. or the Demetrius model. The fact that (at least) two alternative accounts of allometric scaling give opposite predictions in respect of such experiments makes the need for an examination of cultured cells from metabolically active tissues even more crucial.I thank my colleague Dr. Paul Agutter for his comments on this review.REFERENCES1 Agutter PS, Wheatley DN. Metabolic scaling: consensus or controversy? Theoret Biol Med Model 1: 13, 2004.Crossref | PubMed | Google Scholar2 Brown MF, Gratton TP, Stuart JA. Metabolic rate does not scale with body mass in cultured mammalian cells. Am J Physiol Regul Integr Comp Physiol 292: R2115–R2121, 2007.Link | ISI | Google Scholar3 Clegg JS, Wheatley DN. Intracellular organization: evolutionary origins and possible consequences of metabolic rate control in vertebrates. Am Zool 31: 504–513, 1991.Crossref | Google Scholar4 Coulson RA. Metabolic rate and the flow theory: a study in chemical engineering. Comp Biochem Physiol 84: 217–229,1986.Crossref | Google Scholar5 Coulson RA, Hernandez T, Herbert JD. Metabolic rate and enzyme kinetics in vivo. Comp Biochem Physiol 56: 251–262, 1977.Crossref | Google Scholar6 Demetrius L. Quantum statistics and metabolic scaling of organisms. Physica A 322: 477–490, 2003.Crossref | ISI | Google Scholar7 Demetrius L. The origin of allometric scaling laws in biology. J Theor Biol 243: 455–467, 2006.Crossref | PubMed | ISI | Google Scholar8 Glazier DS. Beyond the “3/4-power law”: variation in the intra- and interspecific scaling of metabolic rate in animals. Biol Rev Camb Philos Soc 80: 611–662, 2005.Crossref | PubMed | ISI | Google Scholar9 Krebs H. Body size and tissue respiration. Biochim Biophys Acta 4: 249–269, 1950.Crossref | PubMed | ISI | Google Scholar10 Martin AW, Fuhrman FA. The relationship between summated tissue respiration and metabolic rate in the mouse and dog. Physiol Zool 28: 18–34, 1955.Crossref | Google Scholar11 Porter RK, Brand MD. Cellular oxygen consumption depends on body mass. Am J Physiol Regul Integr Comp Physiol 269: R226–R228, 1995.Link | ISI | Google Scholar12 Wang Z, O'Connor T, Heshk S, Heymsfield SB. The reconstruction of Kleiber's law at the organ-tissue level. J Nutr 131: 2967–2970, 2001.Crossref | PubMed | ISI | Google Scholar13 West GB, Brown JH. The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. J Exp Biol 208: 1575–92, 2005.Crossref | PubMed | ISI | Google Scholar14 West GB, Brown JH, Enquist BJ. A general model for the origin of allometric scaling laws in biology. Science 276: 122–126, 1997.Crossref | PubMed | ISI | Google Scholar15 West GB, Woodruff WH, Brown JH. Allometric scaling of metabolic rate from molecules and mitochondria to cells and mammals. Proc Natl Acad Sci USA 99: 2473–2478, 2002.Crossref | PubMed | ISI | Google Scholar16 Wheatley DN, Clegg JS. What determines the basal metabolic rate of vertebrate cells in vivo? Biosystems 32: 83–92, 1994.Crossref | PubMed | ISI | Google ScholarAUTHOR NOTESAddress for reprint requests and other correspondence: D. Wheatley, BioMedES, Leggat House, Keithhall, nverurie, Aberdeen AB51 0LX, UK (e-mail: [email protected]) Download PDF Back to Top Next FiguresReferencesRelatedInformationCited ByDoes Cellular Metabolism from Primary Fibroblasts and Oxidative Stress in Blood Differ between Mammals and Birds? The (Lack-thereof) Scaling of Oxidative Stress29 April 2019 | Integrative and Comparative Biology, Vol. 59, No. 4Body-Mass Scaling of Metabolic Rate: What are the Relative Roles of Cellular versus Systemic Effects?4 March 2015 | Biology, Vol. 4, No. 1Metabolic Scaling in Complex Living Systems1 October 2014 | Systems, Vol. 2, No. 4Physiological underpinnings associated with differences in pace of life and metabolic rate in north temperate and neotropical birds27 March 2014 | Journal of Comparative Physiology B, Vol. 184, No. 5Mice divergently selected for high and low basal metabolic rates evolved different cell size and organ mass13 January 2014 | Journal of Evolutionary Biology, Vol. 27, No. 3Human cancer cell lines: Experimental models for cancer cells in situ? For cancer stem cells?Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, Vol. 1795, No. 2Fibroblasts From Naked Mole-Rats Are Resistant to Multiple Forms of Cell Injury, But Sensitive to Peroxide, Ultraviolet Light, and Endoplasmic Reticulum StressThe Journals of Gerontology Series A: Biological Sciences and Medical Sciences, Vol. 63, No. 3 More from this issue > Volume 292Issue 6June 2007Pages R2113-R2114 Copyright & PermissionsCopyright © 2007 the American Physiological Societyhttps://doi.org/10.1152/ajpregu.00102.2007PubMed17379845History Published online 1 June 2007 Published in print 1 June 2007 Metrics

Presidential address

This issue commemorates the 10th biannual congress of the European Society for Evolutionary Biology (ESEB). The foundation of the Society in 1987 must have been exactly at the right moment. In retrospect, the state of the field of evolutionary biology in Europe at that time can be compared with a saturated salt solution, requiring just a trigger to crystallize into a coherent structure. It was the neo-European Steve Stearns, then zoology professor at the University of Basel in Switzerland, who possessed the required authority and organizational talent to provide this trigger. The first ESEB congress, held in 1987 in Basel, was immediately a big success, attracting some 450 participants from all over Europe. The next congresses have been held in various European cities and attracted between 500 and 700 participants, with one outlier: Barcelona in 1999 with over 900 attending. The ESEB congresses have increasingly attracted participants from North America. Steve Stearns was also responsible for founding the Journal of Evolutionary Biology (JEB). JEB is now fully owned by ESEB and is published by Blackwell Publishing. Like ESEB, JEB has shown a remarkably successful history. Over the years the number of submitted manuscripts has steadily increased and is still increasing. The journal has established a solid position in the field. Particularly impressive is the sharp reduction in manuscript handling time, thanks to a very dedicated board of reviewing editors. The mean time between submission and final decision is now about 60 days. Parallel to the above mentioned increase of North American participants to the ESEB congresses is the increase in JEB articles from North American authors. I have no doubts that both ESEB and JEB have been very important in stimulating European evolutionary research and in establishing collaboration within Europe. I very much welcome the increasing involvement of North American evolutionary biologists as is apparent from the trends mentioned above. European evolutionary biology is flourishing, although there are signs that also in Europe nonscientific opposition to evolutionary thinking is becoming more vocal. In opposing this ESEB can play a very useful role.

Natal dispersal and personalities in great tits (Parus major).

Dispersal is a major determinant of the dynamics and genetic structure of populations, and its consequences depend not only on average dispersal rates and distances, but also on the characteristics of dispersing and philopatric individuals. We investigated whether natal dispersal correlated with a predisposed behavioural trait: exploratory behaviour in novel environments. Wild great tits were caught in their natural habitat, tested the following morning in the laboratory using an open field test and released at the capture site. Natal dispersal correlated positively with parental and individual exploratory behaviour, using three independent datasets. First, fast-exploring parents had offspring that dispersed furthest. Second, immigrants were faster explorers than locally born birds. Third, post-fledging movements, comprising a major proportion of the variation in natal dispersal distances, were greater for fast females than for slow females. These findings suggest that parental behaviour influenced offspring natal dispersal either via parental behaviour per se (e.g. via post-fledging care) or by affecting the phenotype of their offspring (e.g. via their genes). Because this personality trait has a genetic basis, our results imply that genotypes differ in their dispersal distances. Therefore, the described patterns have profound consequences for the genetic composition of populations.

Sex-biased dispersal in a salmonid fish.

We tested the hypothesis that dispersal is sex biased in an unexploited population of brook trout, Salvelinus fontinalis, on Cape Race, Newfoundland, Canada. Based on the assumptions that trout are promiscuous and that reproductive success is limited primarily by either number of mates (males) or fecundity (females), we predicted that males would disperse greater distances than females. We also tested the hypothesis that trout populations comprise stationary and mobile individuals, predicting that males have greater mobility than females. Based on a mark-recapture study of 943 individually tagged fishes, 191 of which were recaptured over 5 years, we find strong support for our hypothesis of male-biased dispersal in brook trout. Averaged among all 11 resampling periods, males dispersed 2.5 times as far as females; during the spawning period only, male dispersal exceeded that by females almost fourfold. Both sexes were heterogeneous with respect to movement, with a lower incidence of mobility among females (29.6%) than males (41.1%); mobile males dispersed six times further than mobile females. We conclude that this sex bias reduces mate competition among male kin and decreases the probability that males will reproduce with related females.

Dynamic adjustment of parental care in response to perceived paternity.

Theories of parental care evolution predict that genetic relatedness will be an important variable in the amount of care a parent provides. However, current inferences of relatedness-based parental investment from studies in humans and birds remain challenged. No study has yet demonstrated parental care adjustment in a manner uncomplicated by life-history correlates or experimental design. We now present a unique test that controls for individual life histories and demonstrates paternity-related dynamic adjustments in parental care. Brood-rearing male bluegill sunfish (Lepomis macrochirus) that are cuckolded to a varying degree will either increase or decrease their parental investment in response to changing information on paternity during brood development. Specifically, as parental males detect paternity lost to cuckolders and, hence, a reduction in the value of their brood, they adaptively lower their level of parental care. Conversely, if they detect that their paternity is higher than previously assessed, they adaptively raise their level of parental care. This dynamic adjustment during brood rearing indicates the importance of genetic relatedness in parental investment decisions and provides needed empirical support for theoretical predictions.

Conspecific reproductive success affects age of recruitment in a great cormorant, Phalacrocorax carbo sinensis, colony.

Few studies have addressed the proximate factors affecting the age at which individuals of long-lived bird species are recruited into the breeding population. We use capture-recapture analysis of resightings of 16 birth cohorts of colour-ringed great cormorants, Phalacrocorax carbo sinensis, in a Danish colony to assess the evidence for two hypotheses: conspecific attraction (earlier recruitment when the colony is large) and conspecific reproductive success (earlier recruitment following years of high breeding success). For both males and females, conspecific reproductive success was the most important covariate explaining the interannual variation in age of recruitment; colony size was also important for females. These covariates explained nearly 60% of the year-to-year variation for both sexes. The age of recruitment increased for cohorts born after 1990, and this increase was correlated with a decline in breeding success in the colony; we interpret this as an indirect and delayed density-dependent effect. Females were recruited earlier than males (mean age of recruitment for cohorts born before 1990: 2.98 years versus 3.53 years); the most plausible reason for this is a skewed sex ratio in favour of males in the adult population. Recruitment of males may thus, to some extent, be constrained by the availability of females. This study provides the first evidence that conspecific reproductive success can affect the age at which individual birds start to breed.

Rock-scissors-paper and the survival of the weakest.

In the children's game of rock-scissors-paper, players each choose one of three strategies. A rock beats a pair of scissors, scissors beat a sheet of paper and paper beats a rock, so the strategies form a competitive cycle. Although cycles in competitive ability appear to be reasonably rare among terrestrial plants, they are common among marine sessile organisms and have been reported in other contexts. Here we consider a system with three species in a competitive loop and show that this simple ecology exhibits two counter-intuitive phenomena. First, the species that is least competitive is expected to have the largest population and, where there are oscillations in a finite population, to be the least likely to die out. As a consequence an apparent weakening of a species leads to an increase in its population. Second, evolution favours the most competitive individuals within a species, which leads to a decline in its population. This is analogous to the tragedy of the commons, but here, rather than leading to a collapse, the 'tragedy' acts to maintain diversity.

Reversible frequency-dependent switches in male mate choice.

Current sexual-selection theories predict that mating should occur preferentially with the highest-quality partner, and assume that for distinguishing among potential mates the choosy sex applies an internal representation of the characteristics of the desired mate, i.e. a template. Binary choice experiments were performed to test male mate choice between two different female colour morphs in the damselfly Ischnura elegans. Choice experiments were conducted before and after an habituation period, during which males were exposed to only one female colour morph. Given the choice between the two female morphs, males did exhibit a choice for the most recently experienced female morph. This is the first evidence for a reversible switch in mate choice in a frequency-dependent way. In contrast with previous studies on mate choice, template formation in male I. elegans seems not to be based on quality. Switching mate choice in a frequency-dependent manner, choosing the most common morph, probably allows males to minimize their search efforts and to maximize fitness.