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14 Dec 2016
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High Rates of Species Accumulation in Animals with Bioluminescent Courtship Displays

Bioluminescent sexually selected traits as an engine for biodiversity across animal species

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In evolutionary biology, sexual selection is hypothesized to increase speciation rates in animals, as theory predicts that sexual selection will contribute to phenotypic diversification and affect rates of species accumulation at macro-evolutionary time scales. However, testing this hypothesis and gathering convincing evidence have proven difficult. Although some studies have shown a strong correlation between proxies of sexual selection and species diversity (mostly in birds), this relationship relies on some assumptions on the link between these proxies and the strength of sexual selection and is not detected in some other taxa, making taxonomically widespread conclusions impossible.

In a recent study published in Current Biology [1], Ellis and Oakley provide strong evidence that bioluminescent sexual displays have driven high species richness in taxonomically diverse animal lineages, providing a crucial link between sexual selection and speciation.
It was known that bioluminescence has evolved independently more than 40 times, with males often using it as a mating signal but with also some other possible adaptive functions including anti-predator defense and predation. Moreover, it has been reported that small marine lanternfishes and sharks that use bioluminescence in mate identification had a greater concentration of species than other deep-sea fishes that use bioluminescence for defensive purposes [2-4]. But no one had ever determined whether this pattern is consistent across diverse and distantly related animal groups living on sea and land.

Ellis and Oakley [1] explored the scientific literature for well-resolved evolutionary trees with branches containing bioluminescent lineages and identified lineages that use light for courtship or camouflage in a wide range of marine and terrestrial taxa including insects, crustaceans, cephalopods, segmented worms, and fishes. The researchers counted the number of species in each bioluminescent clade and found that all groups with light-courtship displays had more species and faster rates of species accumulation than their non-luminous most closely related sister lineages or ancestors. In contrast, those groups that used bioluminescence for predator avoidance had a lower than expected rate of species richness on average.

Nicely encompassing a diversity of taxa and neatly controlling for the rate of species accumulation of the encompassing clade, the results of Ellis and Oakley are clear-cut and provide the most comprehensive evidence to date for the hypothesis that sexual displays can act as drivers of speciation. One question this study incites is what is happening in terms of sexual selection in species displaying defensive bioluminescence or no bioluminescence at all: do those lineages use no mating signals at all or other mating signals that are less apparent, and will those experience lower levels of sexual selection than bioluminescent mating signals, i.e. consistent with Ellis and Oakley results? It would also be interesting to investigate the diversification rates in animal species using other modalities, such as chemical, acoustic or any other type of signals used by males, females or both sexes, to determine what types of sexual signals may be more generally drivers of speciation.

References

[1] Ellis EA, Oakley TH. 2016. High Rates of Species Accumulation in Animals with Bioluminescent Courtship Displays. Current Biology 26:1916–1921. doi: 10.1016/j.cub.2016.05.043

[2] Davis MP, Holcroft NI, Wiley EO, Sparks JS, Smith WL. 2014. Species-specific bioluminescence facilitates speciation in the deep sea. Marine Biology 161:1139­1148. doi: 10.1007/s00227-014-2406-x

[3] Davis MP, Sparks JS, Smith WL. 2016. Repeated and Widespread Evolution of Bioluminescence in Marine Fishes. PLoS One 11:e0155154. doi: 10.1371/journal.pone.0155154

[4] Claes JM, Nilsson D-E, Mallefet J, Straube N. 2015. The presence of lateral photophores correlates with increased speciation in deep-sea bioluminescent sharks. Royal Society Open Science 2:150219. doi: 10.1098/rsos.150219

High Rates of Species Accumulation in Animals with Bioluminescent Courtship DisplaysEllis EA, Oakley THOne of the great mysteries of evolutionary biology is why closely related lineages accumulate species at different rates. Theory predicts that populations undergoing strong sexual selection will more quickly differentiate because of increased pote...Adaptation, Evolutionary Ecology, Sexual Selection, SpeciationAstrid Groot2016-12-14 19:01:59 View
14 Dec 2016
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Evolution of resistance to single and combined floral phytochemicals by a bumble bee parasite

The medicinal value of phytochemicals is hindered by pathogen evolution of resistance

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As plants cannot run from their enemies, natural selection has favoured the evolution of diverse chemical compounds (phytochemicals) to protect them against herbivores and pathogens. This provides an opportunity for plant feeders to exploit these compounds to combat their own enemies. Indeed, it is widely known that herbivores use such compounds as protection against predators [1]. Recently, this reasoning has been extended to pathogens, and elegant studies have shown that some herbivores feed on phytochemical-containing plants reducing both parasite abundance within hosts [2] and their virulence [3].
Suffering less from parasites is clearly beneficial for infected herbivores. Why then, is this behaviour not fixed in nature? There are, at least, two possible explanations. First, feeding on ‘medicinal’, often toxic, plants may impose costs upon uninfected individuals. Second, parasites may evolve resistance to such chemicals. Whereas the first possibility has been explored, and is taken as evidence for ‘self-medication’ [3], the second hypothesis requires investigation. A recent study by Palmer-Young et al. [4] fills this gap. This article reports evolution of resistance to two different phytochemicals, alone and in combination, in the trypanosome Crithidia bombi, a bumble bee (Bombus impatiens) parasite. To show this, the authors experimentally evolved a strain of C. bombi in the presence of thymol, eugenol or both simultaneously. These phytochemicals are commonly found in the nectar of several plant species, in particular those of the Lamiaceae, a family containing several aromatic herbs. Prior to selection both phytochemicals reduced C. bombi growth by about 50%. However, C. bombi rapidly evolved resistance in both single and the double phytochemical treatments. Moreover, no cost of resistance was detected when evolved parasites were placed in the ancestral, phytochemical-free environment. Therefore, resistance to phytochemicals would be expected to spread rapidly in natural populations of C. bombi. Clearly, thus, the herbivore strategy of sequestering plant secondary chemical compounds as a defence against their pathogens should fail. The question then is ‘why do they still do it’? Can self-medication work in the longer-term for bumblebees?
Well, yes. The very fact that resistance evolved shows that resistance is not fixed in natural C. bombi populations. This is surprising considering that resistance is not costly. This might be due to a number of reasons. Firstly, there may be costs of resistance that were not detected in this experiment. Second, it may not be possible to evolve universal resistance to the heterogeneity present in the phytochemical environment. Indeed, phytochemical environments are highly varied in time and space and bumblebees will visit different plants presenting different phytochemical cocktails throughout the season. Furthermore, migration of bees from populations exposed to different phytochemicals may prevent the fixation of one resistance type.
Or, it may be self-medication behaviour itself that prevents the evolution of resistance? Indeed, in the same way that infected bees seek cooler temperatures to slow growth of a parasitoid fly [5], they may also seek a more varied diet with diverse phytochemicals to which the parasite cannot evolve, but which reduces parasite growth. Further understanding of arthropod self-medication may thus be instrumental to prevent the observed worldwide decline of pollinators [6]. Furthermore, it may inform on mechanisms that prevent rapid evolution of drug resistance in other systems.

References

[1] Duffey SS. 1980. Sequestration of plant natural products by insects. Annual Review of Entomology 25: 447-477. doi: 10.1146/annurev.en.25.010180.002311

[2] Richardson LL et al. 2015. Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proceedings of the Royal Society of London B 282: 20142471. doi: 10.1098/rspb.2014.2471

[3] Lefèvre T et al. 2010. Evidence for trans-generational medication in nature. Ecology Letters 13: 1485-93. doi: 10.1111/j.1461-0248.2010.01537.x

[4] Palmer-Young EC, Sadd BM, Adler LS. 2017. Evolution of resistance to single and combined floral phytochemicals by a bumble bee parasite. Journal of Evolutionary Biology 30: 300-312. doi: 10.1111/jeb.13002

[5] Müller CB, Schmid-Hempel P. 1993. Exploitation of cold temperature as defence against parasitoids in bumblebees. Nature 363: 65-67. doi: 10.1038/363065a0

[6] Potts SG et al. 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25: 345-353. doi: 10.1016/j.tree.2010.01.007

Evolution of resistance to single and combined floral phytochemicals by a bumble bee parasitePalmer-Young EC, Sadd BM, Adler LSRepeated exposure to inhibitory compounds can drive the evolution of resistance, which weakens chemical defence against antagonists. Floral phytochemicals in nectar and pollen have antimicrobial properties that can ameliorate infection in pollinat...Evolutionary EcologyAlison Duncan2016-12-14 16:47:14 View
14 Dec 2016
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The Red Queen lives: epistasis between linked resistance loci

Evidence of epistasis provides further support to the Red Queen theory of host-parasite coevolution

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According to the Red Queen theory of antagonistic host-parasite coevolution, adaptation of parasites to the most common host genotype results in negative frequency-dependent selection whereby rare host genotypes are favoured. Assuming that host resistance relies on a genetic host-parasite (mis)match involving several linked loci, then recombination appears as much more efficient than parthenogenesis in generating new resistant host genotypes. This has long been proposed to explain one of the biggest so-called paradoxes in evolutionary biology, i.e. the maintenance of recombination despite its twofold cost.

Evidence from various study systems indicates that successful infection (and hence host resistance) depends on a genetic match between the parasite’s and the host’s genotype via molecular interactions involving elicitor/receptor mechanisms. However the key assumption of epistasis, i.e. that this genetic host-parasite match involves several linked resistance loci, remained unsupported so far. Metzger and coauthors [1] now provide empirical support for it.

Daphnia magna can reproduce both sexually and clonally and their well-studied interaction with Pasteuria ramosa makes them an excellent model system to investigate the genetics of host resistance. D. magna hosts were found to be either resistant (complete lack of attachment of parasite spores to the host’s foregut) or susceptible (full attachment). In this study the authors carried out an elegant Mendelian genetic investigation by performing multiple crosses between four host genotypes differing in their resistance to two different parasite isolates [1].

Their results show that resistance of D. magna to each of the two P. ramosa isolates relies on Mendelian inheritance at two loci that are linked (A and B), each of them having two alleles with dominant resistance; furthermore resistance to one parasite isolate confers susceptibility to the other. They also show that a third locus appears to confer double resistance (C), but that even double resistant hosts remain susceptible to other parasite isolates, and hence that universal host resistance is lacking – all of this supporting the Red Queen theory.

This paper demonstrates with a high level of clarity that host resistance is governed by multiple linked loci. The assumption of epistasis between resistance loci is supported, which makes it possible for sexual recombination to be maintained by antagonistic host-parasite coevolution.

Reference

[1] Metzger CMJA, Luijckx P, Bento G, Mariadassou M, Ebert D. 2016. The Red Queen lives: epistasis between linked resistance loci. Evolution 70:480-487. doi: 10.1111/evo.12854

The Red Queen lives: epistasis between linked resistance lociMetzger CMJA, Luijckx P, Bento G, Mariadassou M, Ebert D.A popular theory explaining the maintenance of genetic recombination (sex) is the Red Queen Theory. This theory revolves around the idea that time-lagged negative frequency-dependent selection by parasites favors rare host genotypes generated thro...Evolutionary Dynamics, Evolutionary Theory, Reproduction and Sex, Species interactionsAdele Mennerat2016-12-14 13:58:53 View
13 Dec 2016
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Prezygotic isolation, mating preferences, and the evolution of chromosomal inversions

The spread of chromosomal inversions as a mechanism for reinforcement

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Several examples of chromosomal inversions carrying genes affecting mate choice have been reported from various organisms. Furthermore, inversions are also frequently involved in genetic isolation between populations or species. Past work has shown that inversions can spread when they capture not only some loci involved in mate choice but also loci involved in incompatibilities between hybridizing populations [1]. In this new paper [2], the authors derive analytical approximations for the selection coefficient associated with an inversion suppressing recombination between a locus involved in mate choice and one (or several) locus involved in Dobzhansky-Muller incompatibilities. Two mechanisms for mate choice are considered: assortative mating based on the allele present at a single locus, or a trait-preference model where one locus codes for the trait and another for the preference. The results show that such an inversion is generally favoured, the selective advantage associated with the inversion being strongest when hybridization is sufficiently frequent. Assuming pairwise epistatic interactions between loci involved in incompatibilities, selection for the inversion increases approximately linearly with the number of such loci captured by the inversion.

This paper is a good read for several reasons. First, it presents the problem clearly (e.g. the introduction provides a clear and concise presentation of the issue and past work) and its crystal-clear writing facilitates the reader's understanding of theoretical approaches and results. Second, the analysis is competently done and adds to previous work by showing that very general conditions are expected to be favourable to the spread of the type of inversion considered here. And third, it provides food for thought about the role of inversions in the origin or the reinforcement of divergence between nascent species. One result of this work is that an inversion linked to pre-zygotic isolation "is favoured so long as there is viability selection against recombinant genotypes", suggesting that genetic incompatibilities must have evolved first and that inversions capturing mating preference loci may then enhance pre-existing reproductive isolation. However, the results also show that inversions are more likely to be favoured in hybridizing populations among which gene flow is still high, rather than in more strongly isolated populations. This matches the observation that inversions are more frequently observed between sympatric species than between allopatric ones.

References

[1] Trickett AJ, Butlin RK. 1994. Recombination Suppressors and the Evolution of New Species. Heredity 73:339-345. doi: 10.1038/hdy.1994.180

[2] Dagilis AJ, Kirkpatrick M. 2016. Prezygotic isolation, mating preferences, and the evolution of chromosomal inversions. Evolution 70: 1465–1472. doi: 10.1111/evo.12954

Prezygotic isolation, mating preferences, and the evolution of chromosomal inversionsDagilis AJ, Kirkpatrick MChromosomal inversions are frequently implicated in isolating species. Models have shown how inversions can evolve in the context of postmating isolation. Inversions are also frequently associated with mating preferences, a topic that has not been...Adaptation, Evolutionary Theory, Genome Evolution, Hybridization / Introgression, Population Genetics / Genomics, SpeciationDenis Roze2016-12-13 22:11:54 View
13 Dec 2016
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Addicted? Reduced host resistance in populations with defensive symbionts

Hooked on Wolbachia

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This very nice paper by Martinez et al. [1] provides further evidence, if further evidence was needed, of the extent to which heritable microorganisms run the evolutionary show.
Wolbachia is an ubiquitous endosymbiont of arthropods who has been recently shown to protect its hosts against viral infections. Here, Martinez et al. are able to show that this multifaceted heritable symbiont weakens selective pressures induced by viruses on host immune genes. In a series of very elegant experiments, Wolbachia-infected and Wolbachia-free populations of D. melanogaster were exposed to Drosophila C virus (a natural, and highly virulent Drosophila pathogen). At the end of a 9-generation artificial selection protocol with DCV, resistance against DCV increased in flies, both in the presence and absence of Wolbachia. Wolbachia-infected flies were still substantially more resistant to DCV viruses than their Wolbachia-free counterparts. Crucially, however, the frequency of the pastrel resistant allele (a key immune gene for DCV resistance) was significantly lower in the Wolbachia-infected lines. As a consequence, when the DCV-evolved lines were treated with antibiotics to cure them from the bacterial infection, the lines who had evolved with Wolbachia tended to be more susceptible to the virus than their uninfected counterparts.
In other words, infection by protective heritable symbionts can affect how selection acts on the host's nuclear-based resistance, effectively rendering it dependent on its symbiont for the fight against pathogens.
But the interest of these results may not be simply academic. The protective qualities of Wolbachia against a range of pathogens have opened up the exciting possibility of transferring these bacteria to mosquito vectors of key human diseases such as dengue or malaria. The long term evolutionary potential for these novel Wolbachia-host interactions has, however, been little explored. Either the Wolbachia, the pathogen or, as shown here, the host, could evolve in more or less predictable ways. There is, for example, evidence showing that in novel hosts Wolbachia evolves rapidly and tends to gradually lose its virulence. If the lost virulence was to result in a decrease in their pathogen defensive qualities, the mosquito, having lost the efficiency of its conventional immune defences, could end up being more vulnerable to infection than before the Wolbachia introduction. Martinez et al.'s paper is a nice example of how investigating the evolutionary potential of such Wolbachia-host-pathogen interactions can be hugely informative as to the long term prospects of these new control methods.

Reference

[1] Martinez J, Cogni R, Cao C, Smith S, Illingworth CJR & Jiggins FM. 2016. Addicted? Reduced host resistance in populations with defensive symbionts. Proceedings of the Royal Society of London B 283:20160778. doi: 10.1098/rspb.2016.0778

Addicted? Reduced host resistance in populations with defensive symbiontsMartinez J, Cogni R, Cao C, Smith S, Illingworth CJR & Jiggins FMHeritable symbionts that protect their hosts from pathogens have been described in a wide range of insect species. By reducing the incidence or severity of infection, these symbionts have the potential to reduce the strength of selection on genes ...Adaptation, Evolutionary Applications, Evolutionary Ecology, Experimental Evolution, Life HistoryAna Rivero2016-12-13 20:08:37 View
13 Dec 2016
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Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax)

Supergene Control of a Reproductive Polymorphism

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Two back-to-back papers published earlier this year in Nature Genetics provide compelling evidence for the control of a male reproductive polymorphism in a wading bird by a "supergene", a cluster of tightly linked genes [1-2]. The bird in question, the ruff (Philomachus pugnax), has a rather unusual reproductive system that consists of three distinct types of males ("reproductive morphs"): aggressive "independents" who represent the majority of males; a smaller fraction of non-territorial "satellites" who are submissive towards "independents"; and "faeders" who mimic females and are rare. Previous work has shown that the male morphs differ in major aspects of mating and aggression behavior, plumage coloration and body size, and that – intriguingly – this complex multi-trait polymorphism is apparently controlled by a single autosomal Mendelian locus with three alleles [3]. To uncover the genetic control of this polymorphism two independent teams, led by Terry Burke [1] and Leif Andersson [2], have set out to analyze the genomes of male ruffs. Using a combination of genomics and genetics, both groups managed to pin down the supergene locus and map it to a non-recombining, 4.5 Mb large inversion which arose 3.8 million years ago. While "independents" are homozygous for the ancestral uninverted sequence, "satellites" and "faeders" carry evolutionarily divergent, dominant alternative haplotypes of the inversion. Thus, as in several other notable cases, for example the supergene control of disassortative mating, aggressiveness and plumage color in white-throated sparrows [4], of mimicry in Heliconius and Papilio butterflies [5-6], or of social structure in ants [7], an inversion – behaving as a single "locus" – underpins the mechanistic basis of the supergene. More generally, and beyond inversions, a growing number of studies now shows that selection can favor the evolution of suppressed recombination, thereby leading to the emergence of clusters of tightly linked loci which can then control – presumably due to polygenic gene action – a suite of complex phenotypes [8-10]. A largely unresolved question in this field concerns the identity of the causative alleles and loci within a given supergene. Recent progress on this question has been made for example in Papilio polytes butterflies where a mimicry supergene has been found to involve – surprisingly – only a single but large gene: multiple mimicry alleles in the doublesex gene are maintained in strong linkage disequilibrium via an inversion. It will clearly be of great interest to see future examples of such a fine-scale genetic dissection of supergenes. In conclusion, we were impressed by the data and analyses of Küpper et al. [1] and Lamichhaney et al. [2]: both papers beautifully illustrate how genomics and evolutionary ecology can be combined to make new, exciting discoveries. Both papers will appeal to readers with an interest in supergenes, inversions, the interplay of selection and recombination, or the genetic control of complex phenotypes.

References

[1] Küpper C, Stocks M, Risse JE, dos Remedios N, Farrell LL, McRae SB, Morgan TC, Karlionova N, Pinchuk P, Verkuil YI, et al. 2016. A supergene determines highly divergent male reproductive morphs in the ruff. Nature Genetics 48:79-83. doi: 10.1038/ng.3443

[2] Lamichhaney S, Fan G, Widemo F, Gunnarsson U, Thalmann DS, Hoeppner MP, Kerje S, Gustafson U, Shi C, Zhang H, et al. 2016. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nature Genetics 48:84-88. doi: 10.1038/ng.3430

[3] Lank DB, Smith CM, Hanotte O, Burke T, Cooke F. 1995. Genetic polymorphism for alternative mating behaviour in lekking male ruff Philomachus pugnax. Nature 378:59-62. doi: 10.1038/378059a0

[4] Tuttle Elaina M, Bergland Alan O, Korody Marisa L, Brewer Michael S, Newhouse Daniel J, Minx P, Stager M, Betuel A, Cheviron Zachary A, Warren Wesley C, et al. 2016. Divergence and Functional Degradation of a Sex Chromosome-like Supergene. Current Biology 26:344-350. doi: 10.1016/j.cub.2015.11.069

[5] Joron M, Frezal L, Jones RT, Chamberlain NL, Lee SF, Haag CR, Whibley A, Becuwe M, Baxter SW, Ferguson L, et al. 2011. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477:203-206. doi: 10.1038/nature10341

[6] Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A, Reed RD, Mullen SP, Kronforst MR. 2014. doublesex is a mimicry supergene. Nature 507:229-232. doi: 10.1038/nature13112

[7] Wang J, Wurm Y, Nipitwattanaphon M, Riba-Grognuz O, Huang Y-C, Shoemaker D, Keller L. 2013. A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493:664-668. doi: 10.1038/nature11832

[8] Thompson MJ, Jiggins CD. 2014. Supergenes and their role in evolution. Heredity 113:1-8. doi: 10.1038/hdy.2014.20

[9] Schwander T, Libbrecht R, Keller L. 2014. Supergenes and Complex Phenotypes. Current Biology 24:R288-R294. doi: 10.1016/j.cub.2014.01.056

[10] Charlesworth D. 2015. The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations. Evolutionary Applications 9:74-90. doi: 10.1111/eva.12291

Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax)Lamichhaney S, Fan G, Widemo F, Gunnarsson U, Thalmann DS, Hoeppner MP, Kerje S, Gustafson U, Shi C, Zhang H, et al.The ruff is a Palearctic wader with a spectacular lekking behavior where highly ornamented males compete for females1, 2, 3, 4. This bird has one of the most remarkable mating systems in the animal kingdom, comprising three different male morphs (...Adaptation, Behavior & Social Evolution, Genotype-Phenotype, Life History, Population Genetics / Genomics, Quantitative Genetics, Reproduction and SexThomas Flatt2016-12-13 17:46:54 View
13 Dec 2016
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A supergene determines highly divergent male reproductive morphs in the ruff

Supergene Control of a Reproductive Polymorphism

Recommended by and

Two back-to-back papers published earlier this year in Nature Genetics provide compelling evidence for the control of a male reproductive polymorphism in a wading bird by a "supergene", a cluster of tightly linked genes [1-2]. The bird in question, the ruff (Philomachus pugnax), has a rather unusual reproductive system that consists of three distinct types of males ("reproductive morphs"): aggressive "independents" who represent the majority of males; a smaller fraction of non-territorial "satellites" who are submissive towards "independents"; and "faeders" who mimic females and are rare. Previous work has shown that the male morphs differ in major aspects of mating and aggression behavior, plumage coloration and body size, and that – intriguingly – this complex multi-trait polymorphism is apparently controlled by a single autosomal Mendelian locus with three alleles [3]. To uncover the genetic control of this polymorphism two independent teams, led by Terry Burke [1] and Leif Andersson [2], have set out to analyze the genomes of male ruffs. Using a combination of genomics and genetics, both groups managed to pin down the supergene locus and map it to a non-recombining, 4.5 Mb large inversion which arose 3.8 million years ago. While "independents" are homozygous for the ancestral uninverted sequence, "satellites" and "faeders" carry evolutionarily divergent, dominant alternative haplotypes of the inversion. Thus, as in several other notable cases, for example the supergene control of disassortative mating, aggressiveness and plumage color in white-throated sparrows [4], of mimicry in Heliconius and Papilio butterflies [5-6], or of social structure in ants [7], an inversion – behaving as a single "locus" – underpins the mechanistic basis of the supergene. More generally, and beyond inversions, a growing number of studies now shows that selection can favor the evolution of suppressed recombination, thereby leading to the emergence of clusters of tightly linked loci which can then control – presumably due to polygenic gene action – a suite of complex phenotypes [8-10]. A largely unresolved question in this field concerns the identity of the causative alleles and loci within a given supergene. Recent progress on this question has been made for example in Papilio polytes butterflies where a mimicry supergene has been found to involve – surprisingly – only a single but large gene: multiple mimicry alleles in the doublesex gene are maintained in strong linkage disequilibrium via an inversion. It will clearly be of great interest to see future examples of such a fine-scale genetic dissection of supergenes. In conclusion, we were impressed by the data and analyses of Küpper et al. [1] and Lamichhaney et al. [2]: both papers beautifully illustrate how genomics and evolutionary ecology can be combined to make new, exciting discoveries. Both papers will appeal to readers with an interest in supergenes, inversions, the interplay of selection and recombination, or the genetic control of complex phenotypes.

References

[1] Küpper C, Stocks M, Risse JE, dos Remedios N, Farrell LL, McRae SB, Morgan TC, Karlionova N, Pinchuk P, Verkuil YI, et al. 2016. A supergene determines highly divergent male reproductive morphs in the ruff. Nature Genetics 48:79-83. doi: 10.1038/ng.3443

[2] Lamichhaney S, Fan G, Widemo F, Gunnarsson U, Thalmann DS, Hoeppner MP, Kerje S, Gustafson U, Shi C, Zhang H, et al. 2016. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nature Genetics 48:84-88. doi: 10.1038/ng.3430

[3] Lank DB, Smith CM, Hanotte O, Burke T, Cooke F. 1995. Genetic polymorphism for alternative mating behaviour in lekking male ruff Philomachus pugnax. Nature 378:59-62. doi: 10.1038/378059a0

[4] Tuttle Elaina M, Bergland Alan O, Korody Marisa L, Brewer Michael S, Newhouse Daniel J, Minx P, Stager M, Betuel A, Cheviron Zachary A, Warren Wesley C, et al. 2016. Divergence and Functional Degradation of a Sex Chromosome-like Supergene. Current Biology 26:344-350. doi: 10.1016/j.cub.2015.11.069

[5] Joron M, Frezal L, Jones RT, Chamberlain NL, Lee SF, Haag CR, Whibley A, Becuwe M, Baxter SW, Ferguson L, et al. 2011. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477:203-206. doi: 10.1038/nature10341

[6] Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A, Reed RD, Mullen SP, Kronforst MR. 2014. doublesex is a mimicry supergene. Nature 507:229-232. doi: 10.1038/nature13112

[7] Wang J, Wurm Y, Nipitwattanaphon M, Riba-Grognuz O, Huang Y-C, Shoemaker D, Keller L. 2013. A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493:664-668. doi: 10.1038/nature11832

[8] Thompson MJ, Jiggins CD. 2014. Supergenes and their role in evolution. Heredity 113:1-8. doi: 10.1038/hdy.2014.20

[9] Schwander T, Libbrecht R, Keller L. 2014. Supergenes and Complex Phenotypes. Current Biology 24:R288-R294. doi: 10.1016/j.cub.2014.01.056

[10] Charlesworth D. 2015. The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations. Evolutionary Applications 9:74-90. doi: 10.1111/eva.12291

A supergene determines highly divergent male reproductive morphs in the ruffKüpper C, Stocks M, Risse JE, dos Remedios N, Farrell LL, McRae SB, Morgan TC, Karlionova N, Pinchuk P, Verkuil YI, et al.Three strikingly different alternative male mating morphs (aggressive 'independents', semicooperative 'satellites' and female-mimic 'faeders') coexist as a balanced polymorphism in the ruff, *Philomachus pugnax*, a lek-breeding wading bird1, 2, 3....Adaptation, Genotype-Phenotype, Life History, Population Genetics / Genomics, Reproduction and SexThomas Flatt2016-12-13 17:28:13 View
13 Dec 2016
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Repeated replacements of an intrabacterial symbiont in the tripartite nested mealybug symbiosis

Obligate dependence does not preclude changing partners in a Russian dolls symbiotic system

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Symbiotic associations with bacterial partners have facilitated important evolutionary transitions in the life histories of eukaryotes. For instance, many insects have established long-term interactions with intracellular bacteria that provide them with essential nutrients lacking in their diet. However, despite the high level of interdependency among organisms involved in endosymbiotic systems, examples of symbiont replacements along the evolutionary history of insect hosts are numerous. In their paper, Husnik and McCutcheon [1] test the stability of symbiotic systems in a particularly imbricated Russian-doll type interaction, where one bacterium lives insides another bacterium, which itself lives inside insect cells. For their study, they chose representative species of mealybugs (Pseudococcidae), a species rich group of sap-feeding insects that hosts diverse and complex symbiotic systems. In species of the subfamily Pseudococcinae, data published so far suggest that the primary symbiont, a ß-proteobacterium named Tremblaya princeps, is supplemented by a second bacterial symbiont (a ϒ-proteobaterium) that lives within its cytoplasm; both participate to the metabolic pathways that provide essential amino acids and vitamins to their hosts. Here, Husnik and McCutcheon generate host and endosymbiont genome data for five phylogenetically divergent species of Pseudococcinae in order to better understand: 1) the evolutionary history of the symbiotic associations; 2) the metabolic roles of each partner, 3) the timing and origin of Horizontal Gene Transfers (HGT) between the hosts and their symbionts.
Their results show that all species harbour the primary and at least one secondary symbiont, whose intra-bacterial localization was verified using fluorescence in situ hybridization. In one species (Pseudococcus longispinus), Tremblaya even hosts two intracellular bacteria each with a large genome (even though it is not entirely clear whether these two symbionts are indeed found within Tremblaya). The obligate presence of an intra-bacterial symbiont is best explained by the loss in Tremblaya princeps of critical genes for translation that require “intracellular complementation”.
The most striking result concerns the identity of the intra-bacterial symbiont: genome sizes and structures of the “secondary” (intra-Tremblaya) symbionts vary drastically according to the host species. Phylogenetic analyses based on 80 conserved proteins, place all these ϒ-proteoacteria (except one of the P. longispinus symbionts) in a Sodalis allied clade. However, their relationships do not mirror the one of their hosts, and some of them show signs of very recent acquisition. Altogether these results provide strong evidence for several independent acquisitions of these highly intra-bacterial integrated symbionts. Scenarios for the history of the symbiosis are clearly laid out and discussed by the authors, and the scenario involving several independent replacements of a the intra-Tremblaya symbiont by diverse Sodalis-like bacteria appears the most likely given the data presented here. Selected biosynthetic functions are then mapped onto the host and symbiont genomes, showing the high level of interdependency of the partners for the synthesis of essential amino acids and vitamin. These maps also identify genes in the host genome that might have been acquired through HGT from bacteria and show that many of them are shared by all mealybug species sequenced so far. HGT events have thus predated the acquisitions of the current “intra-Tremblaya“ symbionts and have probably been acquired from previous symbiont infections.
Overall, this is a thorough study, using a diverse set of data and meticulous analyses that present convincing evidence that replacements of symbionts occurred repeatedly even in an imbricated symbiotic system. The phylogenetic analyses inferring the timing of HGTs also depict a highly dynamic history of gene losses and retentions in both host and symbiont genomes. Altogether these results demonstrate how the chimeric nature of individuals allows shuffling at different levels of organisation: organisms like symbionts can be replaced, genes can be exchanged among the partners of the chimera. The surprise is that constraints arising from interdependencies do not impede these exchanges. In the discussion, the authors present a very interesting parallel with the evolution of organelles: if the story presented here mirrors the one of mitochondria, it supports a gradualist view where mitochondria arrived late in the evolution of eukaryotic cells that already contained many bacterial genes resulting from HGT from previous symbionts.

Reference

[1] Husnik F., McCutcheon JP. 2016. Repeated replacements of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. PNAS 113: E5416-E5424. doi: 10.1073/pnas.1603910113

Repeated replacements of an intrabacterial symbiont in the tripartite nested mealybug symbiosisHusnik F, McCutcheon JPStable endosymbiosis of a bacterium into a host cell promotes cellular and genomic complexity. The mealybug *Planococcus citri* has two bacterial endosymbionts with an unusual nested arrangement: the γ-proteobacterium *Moranella endobia* lives in ...Phylogenetics / Phylogenomics, Species interactionsEmmanuelle Jousselin2016-12-13 14:27:09 View