Drosophila sex combs as a model of evolutionary innovations

The diversity of animal and plant forms is shaped by nested evolutionary innovations. Understanding the genetic and molecular changes responsible for these innovations is therefore one of the key goals of evolutionary biology. From the genetic point of view, the origin of novel traits implies the origin of new regulatory pathways to control their development. To understand how these new pathways are assembled in the course of evolution, we need model systems that combine relatively recent innovations with a powerful set of genetic and molecular tools. One such model is provided by the Drosophila sex comb—a male‐specific morphological structure that evolved in a relatively small lineage related to the model species D. melanogaster. Our extensive knowledge of sex comb development in D. melanogaster provides the basis for investigating the genetic changes responsible for sex comb origin and diversification. At the same time, sex combs can change on microevolutionary timescales and differ spectacularly among closely related species, providing opportunities for direct genetic analysis and for integrating developmental and population‐genetic approaches. Sex comb evolution is associated with the origin of novel interactions between Hox and sex determination genes. Activity of the sex determination pathway was brought under the control of the Hox code to become segment‐specific, while Hox gene expression became sexually dimorphic. At the same time, both Hox and sex determination genes were integrated into the intrasegmental spatial patterning network, and acquired new joint downstream targets. Phylogenetic analysis shows that similar sex comb morphologies evolved independently in different lineages. Convergent evolution at the phenotypic level reflects convergent changes in the expression of Hox and sex determination genes, involving both independent gains and losses of regulatory interactions. However, the downstream cell‐differentiation programs have diverged between species, and in some lineages, similar adult morphologies are produced by different morphogenetic mechanisms. These features make the sex comb an excellent model for examining not only the genetic changes responsible for its evolution, but also the cellular processes that translate DNA sequence changes into morphological diversity. The origin and diversification of sex combs provides insights into the roles of modularity, cooption, and regulatory changes in evolutionary innovations, and can serve as a model for understanding the origin of the more drastic novelties that define higher order taxa.     

Polyphyly of Lordiphosa and its relationships in Drosophilinae (Diptera: Drosophilidae)

The phylogenetic relationships of Lordiphosa and some taxa in Drosophilinae were analysed on the basis of a total of forty‐one selected drosophilid species. These included eighteen species of five Lordiphosa species‐groups as the main target, twenty‐three species representative of the major drosophiline ingroup taxa and four species of Steganinae as outgroup. Sixty‐eight morphological characters of adults were subjected to cladistic analysis. From the results it is concluded that Lordiphosa is polyphyletic; the Lo. tenuicauda species‐group and genus Nesiodrosophila form a single monophyletic group; Lordiphosa proper (i.e. Lordiphosa spp. minus the tenuicauda group) comprises another monophyletic group; within Lordiphosa proper the fenestrarum, nigricolor and denticeps groups are all monophyletic, but monophyly of the miki group is not strongly supported; genera Hirtodrosophila and Scaptomyza and subgenus Sophophora are all monophyletic; and within Drosophilinae, genus Scaptodrosophila is the first to have split from the main lineage, but the branching order of other clades, Chymomyza, Lordiphosa proper, Sophophora, Hirtodrosophila, Nesiodrosophila+ Lo. tenuicauda group, Scaptomyza, Dorsilopha and subgenus Drosophila, remains unresolved. The topology of maximum parsimony cladograms suggests that Lordiphosa proper lies close to Sophophora as proposed previously, although its phylogenetic position could not be determined conclusively. By contrast, bootstrap values tended to contradict another hypothesis that Lordiphosa and Scaptomyza are sister groups.     

Phylogenetic Position of the Subgenus Lordiphosa of the Genus Drosophila (Diptera: Drosophilidae) Inferred from Alcohol Dehydrogenase (Adh) Gene Sequences

We analyzed the phylogenetic relationship between the species of Lordiphosa and other Drosophilidae using alcohol dehydrogenase (Adh) gene sequences. The phylogenetic trees consistently show that the four species Drosophila kurokawai, D. collinella, D. stackelbergi, and D. clarofinis, which include three species groups of Lordiphosa, form a monophyletic clade. This clade is placed as a sister group to the willistoni and saltans groups of Sophophora. On the other hand, three species of Lordiphosa, D. tenuicauda, D. pseudotenuicauda, and D. acutissima, all of which belong to the tenuicauda group, are not shown to be related to the major Lordiphosa lineage. In the phylogenetic trees, these species are included into the clade comprised of Drosophila and Hirtodrosophila, although it remains uncertain whether the tenuicauda group is a monophyletic group or not. These results indicate that Lordiphosa is polyphyletic and that most of the members of the subgenus have a close relationship to the neotropical groups of Sophophora. The above conclusion is compatible with the hypothesis of Okada (Mushi [1963] 37:79–100) and Lastovka and Máca (Acta Ent Bohemoslov [1978] 75:404–420) that Lordiphosa is most closely related to Sophophora; in contrast, our results contradict the hypothesis of Grimaldi (Bull Am Mus Nat Hist [1990] 197:1–139) that Lordiphosa is a sister group to the genus Scaptomyza. Received: 12 May 1999 / Accepted: 14 April 2000     

Sex‐biased transcriptome divergence along a latitudinal gradient

Sex‐dependent gene expression is likely an important genomic mechanism that allows sex‐specific adaptation to environmental changes. Among Drosophila species, sex‐biased genes display remarkably consistent evolutionary patterns; male‐biased genes evolve faster than unbiased genes in both coding sequence and expression level, suggesting sex differences in selection through time. However, comparatively little is known of the evolutionary process shaping sex‐biased expression within species. Latitudinal clines offer an opportunity to examine how changes in key ecological parameters also influence sex‐specific selection and the evolution of sex‐biased gene expression. We assayed male and female gene expression in Drosophila serrata along a latitudinal gradient in eastern Australia spanning most of its endemic distribution. Analysis of 11 631 genes across eight populations revealed strong sex differences in the frequency, mode and strength of divergence. Divergence was far stronger in males than females and while latitudinal clines were evident in both sexes, male divergence was often population specific, suggesting responses to localized selection pressures that do not covary predictably with latitude. While divergence was enriched for male‐biased genes, there was no overrepresentation of X‐linked genes in males. By contrast, X‐linked divergence was elevated in females, especially for female‐biased genes. Many genes that diverged in D. serrata have homologs also showing latitudinal divergence in Drosophila simulans and Drosophila melanogaster on other continents, likely indicating parallel adaptation in these distantly related species. Our results suggest that sex differences in selection play an important role in shaping the evolution of gene expression over macro‐ and micro‐ecological spatial scales.     

Dynamic colonization exchanges between continents and islands drive diversification in paradise‐flycatchers (Terpsiphone,Monarchidae)

Aim We use parametric biogeographical reconstruction based on an extensive DNA sequence dataset to characterize the spatio‐temporal pattern of colonization of the Old World monarch flycatchers (Monarchidae). We then use this framework to examine the role of dispersal and colonization in their evolutionary diversification and to compare plumages between island and continental Terpsiphone species. Location Africa, Asia and the Indian Ocean. Methods We generate a DNA sequence dataset of 2300 bp comprising one nuclear and three mitochondrial markers for 89% (17/19) of the Old World Monarchidae species and 70% of the Terpsiphone subspecies. By applying maximum likelihood and Bayesian phylogenetic methods and implementing a Bayesian molecular clock to provide a temporal framework, we reveal the evolutionary history of the group. Furthermore, we employ both Lagrange and Bayes‐ Lagrange analyses to assess ancestral areas at each node of the phylogeny. By combining the ancestral area reconstruction with information on plumage traits we are able to compare patterns of plumage evolution on islands and continents. Results We provide the first comprehensive molecular phylogenetic reconstruction for the Old World Monarchidae. Our phylogenetic results reveal a relatively recent diversification associated with several dispersal events within this group. Moreover, ancestral area analyses reveal an Asian origin of the Indian Ocean and African clades. Ancestral state reconstruction analyses of plumage characters provide an interpretation of the plumage differentiation on islands and continents. Ancestral plumage traits are inferred to be close to those of the Asian paradise‐flycatcher (Terpsiphone paradisi), and island species display a high degree of plumage autapomorphy compared with continental species. Main conclusions Terpsiphone paradisi is polyphyletic and comprises populations that have retained the ancestral plumage of the widespread Terpsiphone genus. The genus appears to have colonized south‐west Asia, the Indian Ocean and Africa from eastern Asia. The phylogeny and divergence time estimates indicate multiple simultaneous colonizations of the western Old World by Terpsiphone. These results reinforce a hypothesis of range expansions of a Terpsiphone paradisi‐like ancestor into eastern Asia and the western Old World.     

Phylogenetic Separation in Limb Use in Captive Gibbons (Hylobatidae): A Comparison Across the Primate Order

Although there have been few studies of self‐scratching in primates, some have reported distinct differences in whether hands or feet are used, and these variations seem to reflect the evolutionary history of the Order. Monkeys and prosimians use both hands and feet to self‐scratch while African great apes use hands almost exclusively. Gibbons represent an evolutionary divergence between monkeys and great apes and incidental observations at the Gibbon Conservation Center pointed to a difference in self‐scratching among the four extant gibbon genera (Hoolock, Nomascus, Symphalangus, and Hylobates). To validate and further explore these preliminary observations, we collected systematic data on self‐scratching from 32 gibbons, including nine species and all four genera. To supplement gibbon data, we also collected self‐scratching information from 18 great apes (four species), five prosimians (two species), 26 New World Monkeys (nine species) and 20 Old World Monkeys (seven species). All monkeys and some prosimians used both hands and feet to self‐scratch, whereas one prosimian species used only feet. All African great apes used hands exclusively (orangutans were an exception displaying occasional foot‐use). This appears to represent a fundamental difference between monkeys and great apes in limb use. Interestingly, there was a clear difference in self‐scratching between the four gibbon genera. Hylobates and Symphalangus self‐scratched only with hands (like all African great apes), while Hoolock and Nomascus self‐scratched with both hands and feet (like monkeys and prosimians). This difference in gibbon behavior may reflect the evolutionary history of gibbons as Hoolock and Nomascus are thought to have evolved before both Hylobates and Symphalangus. What evolutionary pressures led to this divergent pattern is currently opaque; however, this shift in limb preference may result from niche separation across the order facilitating differences in the behavioral repertoire associated with hind and forelimbs. Am. J. Primatol. 74:1035‐1043, 2012. © 2012 Wiley Periodicals, Inc.     

Repeated trans-Atlantic dispersal catalysed a global songbird radiation

Aim Turdus thrushes are one of the most speciose and widespread songbird genera, comprising nearly 70 species that combined have a near‐global distribution. Herein, we use molecular phylogenetic, molecular clock and behavioural evidence to examine the historical biogeography of the genus. Ancestral area reconstructions in conjunction with divergence estimates and palaeoclimatogical data are used to test whether the long‐standing paradigm of Beringian colonization or trans‐Atlantic dispersal best explains modern distributions in the New and Old Worlds. Location Worldwide, with emphasis on New World–Old World biotic interchange. Methods Using a molecular phylogenetic hypothesis of Turdus thrushes, we reconstructed ancestral area relationships utilizing the five major continental or regional areas occupied by species in the genus. We also examined the evolution of behaviours on the phylogeny, and estimated the timing of major lineage divergences via a molecular clock. Results Turdus originated in Eurasia, and following the colonization of Africa underwent a series of five trans‐Atlantic sweepstake dispersals. The data reject the alternative hypothesis that connections between Old and New World Turdus species can be attributed to movement through Beringia with subsequent extinction. Divergence estimates indicate that these dispersals all occurred near the Miocene–Pliocene boundary, 5 Ma. A significant phylogenetic correlation between migratory and flocking behaviour is evident in the genus. Main conclusions The initial divergence of Turdus in the Old World was followed by a series of trans‐Atlantic sweepstake dispersal events. These dispersals are temporally correlated with a specific palaeoclimatic system, which would have facilitated transport of Turdus from the Caribbean to the Old World across the Atlantic. Uplift of the Central American Seaway 4.7 Ma effectively shut down the palaeoclimatic system, and no additional trans‐Atlantic dispersals are evident in Turdus after this time. Migratory movements by ancestral lineages in flocks, rather than as single individuals, suggest an increased likelihood of successfully colonizing new areas, post‐dispersal.     

Sex differences in incubation behaviour but not mortality risk in a threatened shorebird

Sex‐related variation in survival is common in birds and, as it influences effective population size and population growth, is important for conservation and species management. Here we assessed incubation behaviour and sex‐related survival in a threatened sexually monomorphic shorebird, the St Helena Plover Charadrius sanctaehelenae. Males incubated at night, the period of highest activity of cats, which are likely to be predators of breeding birds. In spite of behavioural differences between the sexes, adult survival was not significantly different between males and females, suggesting that sex‐biased behaviour need not lead to sex‐related survival, and thus behavioural differences may not impact upon the adult sex ratio.     

Synonymy of Etiennea Matile-Ferrero with Hemilecanium Newstead (Hemiptera: Coccidae), based on morphology of adult females, adult males and first-instar nymphs, and description of a new potential pest species from the Ryukyu Archipelago, Japan

The genus Etiennea Matile‐Ferrero is synonymized with Hemilecanium Newstead (Hemiptera: Coccidae). We base this decision on a morphological comparative study of adult females, adult males and first‐instar nymphs (crawlers), including a phylogenetic analysis. We recovered a sister group relationship between the type species of the two genera, Etiennea villiersi Matile‐Ferrero and Hemilecanium theobromae Newstead; that is, each was more closely related to the other than either was to other species in their respective genera. All species hitherto included in Etiennea are transferred to Hemilecanium: H. bursera (Hodgson & Kondo) comb. nov., H. cacao (Hodgson) comb. nov., H. candelabra (Hodgson) comb. nov., H. capensis (Hodgson) comb. nov., H. carpenteri (Newstead) comb. nov., H. cephalomeatus (Hodgson) comb. nov., H. combreti (Hodgson) comb. nov., H. ferina (De Lotto) comb. nov., H. ferox (Newstead) comb. nov., H. gouligouli (Hodgson) comb. nov., H. halli (Hodgson) comb. nov., H. kellyi (Brain) comb. nov., H. madagascariensis (Hodgson) comb. nov., H. montrichardiae (Newstead) comb. nov., H. multituberculum (Hodgson) comb. nov., H. petasus (Hodgson) comb. nov., H. sinetuberculum (Hodgson) comb. nov., H. tafoensis (Hodgson) comb. nov., H. ulcusculum (Hodgson) comb. nov., and H. villiersi (Matile‐Ferrero) comb. nov. Keys to the adult females of all 26 species and known adult males and first‐instar nymphs are provided. The adult males and first‐instar nymphs of H. theobromae Newstead and E. villiersi Matile‐Ferrero are for the first time fully described and illustrated. One new potential pest species of Hemilecanium, H. uesatoi Kondo & Hardy sp. nov., which was collected on three islands of the Ryukyu Archipelago, Japan, is described and illustrated based on the adult female, adult male and first‐instar nymph. We discuss evidence that H. uesatoi is a new introduction to the Ryukyu Archipelago. The first‐instar nymphs of Hemilecanium can be divided into two distinct morphological groups, the petasus group and the theobromae group.     

Old World camels in a modern world – a balancing act between conservation and genetic improvement

Old World camels have served humans in cross‐continental caravans, transporting people and goods, connecting different cultures and providing milk, meat, wool and draught since their domestication around 3000–6000 years ago. In a world of modern transport and fast connectivity, these beasts of burden seem to be out‐dated. However, a growing demand for sustainable milk and meat production, especially in countries affected by climate change and increasing desertification, brings dromedaries (Camelus dromedarius) and Bactrian camels (Camelus bactrianus) back onstage and into the focus of animal breeders and scientists. In this review on the molecular genetics of these economically important species we give an overview about the evolutionary history, domestication and dispersal of Old World camels, whereas highlighting the need for conservation of wild two‐humped camels (Camelus ferus) as an evolutionarily unique and highly endangered species. We provide cutting‐edge information on the current molecular resources and on‐going sequencing projects. We cannot emphasise enough the importance of balancing the need for improving camel production traits with maintaining the genetic diversity in two domestic species with specific physiological adaptation to a desert environment.     

Sex-specific methylation in <Emphasis Type="Italic">Drosophila</Emphasis>: an investigation of the <Emphasis Type="Italic">Sophophora</Emphasis> subgenus

Epigenetic phenomena have been widely characterized in the genomes of vertebrates and DNA methylation is a key mechanism of epigenetic regulation. The DNA methylation systems of invertebrates and vertebrates show several notable differences. However, the evolutionary implications of those differences only recently began to be revealed. Our study investigated the recurrence of sex-specific methylation, as previously described for the species Drosophila willistoni, in other species of the Sophophora subgenus that present close evolutionary relationship. The MSRE and Southern blot techniques were used to analyze rDNA of some species of the willistoni, melanogaster, saltans and obscura groups of Drosophila and the results suggested that differential DNA methylation between sexes only occurs in Drosophila tropicalis and D. insularis, two sibling species of the willistoni subgroup. However, only using the MSRE technique we could detect sex-specific patterns of DNA methylation in all species of willistoni subgroup. These results indicate that DNA methylation may present important differences, even between closely related species, shedding new light on this Neotropical species complex.     

Sex-specific expression of a HOX gene associated with rapid morphological evolution

Animal diversity is shaped by the origin and diversification of new morphological structures. Many examples of evolutionary innovations are provided by male-specific traits involved in mating and sexual selection. The origin of new sex-specific characters requires the evolution of new regulatory interactions between sex-determining genes and genes that control spatial patterning and cell differentiation. Here, we show that sex-specific regulation of the HOX gene Sex combs reduced (Scr) is associated with the origin and evolution of the Drosophila sex comb — a novel and rapidly diversifying male-specific organ. In species that primitively lack sex combs, Scr expression shows little spatial modulation, whereas in species that have sex combs, Scr is upregulated in the presumptive sex comb region and is frequently sexually dimorphic. Phylogenetic analysis shows that sex-specific regulation of Scr has been gained and lost multiple times in Drosophila evolution and correlates with convergent origin of similar sex comb morphologies in several independent lineages. Some of these transitions occurred on microevolutionary timescales, indicating that HOX gene expression can evolve with surprising ease. This is the first example of a sex-specific regulation of a HOX gene contributing to the development and evolution of a secondary sexual trait.     

CHROMOSOME NUMBERS AND EVOLUTION IN NORTH AMERICAN SPECIES OF LINUM

Among the North American species of Linum there are three basic chromosome numbers representing invasions from the Old World of three distinct evolutionary lines. N = 9 is found only in the blue-flowered group represented in North America by two species, L. lewisii and L. pratense which are closely related to and may be conspecific with the Old World L. perenne. The basic number for the yellow-flowered species is n = 18 which is characteristic of the Scabrella and Virginiana subgroups. The loss of chromosomes in the Neo-mexicana (n = 13) and Sulcata-Rigida (n = 15) subgroups suggests that the basic haploid number of 18 might be a polyploid derivative of an Old World ancestor with n = 9. The incidence of n = 9 among Old World species of Linum may indicate that this represents an ancestral condition. Linum catharticum has n = 8; this number and features of morphology and distribution suggest that it is not directly related to either the blue-flowered or yellow-flowered groups in North America but represents a separate introduction on this continent.     

Social structure,infant handling,and mothering styles in group-living old world monkeys

I argue that in Old World monkeys, infant handling by individuals other than the mother is a heterogeneous phenomenon in structural and functional terms; species differences in maternal tolerance of infant handling are related to differences in the relative proportion of abusive to affiliative responses made to infants by adult females other than the mother; and infant handling by adult females is related to the species-typical social structure, with particular reference to social relationships among females and patterns of food competition. I apply the proposed relationship among social structure, infant handling, and mothering style to explain the observed variation in mothering styles between and within the subfamilies Colobinae and Cercopithecinae.     

How Drosophila change their combs: the Hox gene Sex combs reduced and sex comb variation among Sophophora species

SUMMARY Identification of the events responsible for rapid morphological variation during evolution can help understand how developmental processes are changed by genetic modifications and thus produce diverse body features and shapes. Sex combs, a sexually dimorphic structure, show considerable variation in morphology and numbers among males from related species of Sophophora , a subgenus of Drosophila . To address which evolutionary changes in developmental processes underlie this diversity, we first analyzed the genetic network that controls morphogenesis of a single sex comb in the model D. melanogaster . We show that it depends on positive and negative regulatory inputs from proximo-distal identity specifying genes, including dachshund, bric à brac , and sex combs distal . All contribute to spatial regulation of the Hox gene Sex combs reduced (Scr ), which is crucial for comb formation. We next analyzed the expression of these genes in sexually dimorphic species with different comb numbers. Only Scr shows considerable expression plasticity, which is correlated with comb number variation in these species. We suggest that differences in comb numbers reflect changes of Scr expression in tarsus primordia, and discuss how initial comb formation could have occurred in an ancestral Sophophora fly following regulatory modifications of developmental programs both parallel to and downstream of Scr .     

Convergent evolution of sunbird pollination systems of Impatiens species in tropical Africa and hummingbird systems of the New World

The bird pollination systems of the New and Old Worlds evolved independently, and differ in many aspects. New World plants are often presented as those adapted to hovering birds while Old World plants to perching birds. Most Neotropical studies also demonstrate that in hummingbird species rich assemblages, only a small number of highly specialized birds exploits the most specialized plants with long corollas. Nevertheless, recent research on bird–plant pollination interactions suggest that sunbird pollination systems in the Old World have converged more with the highly specialized hummingbird pollination systems than previously thought. In this study we focus on the pollination systems of the bird pollination syndrome Impatiens species on Mt. Cameroon, West Africa. We show that despite the high diversity of sunbirds on Mt. Cameroon, only Cyanomitra oritis appear to be important pollinator of all Impatiens species. This asymmetry indicates the absence of pair wise co‐evolution and points to a diffuse co‐evolutionary process resulting in guilds of highly specialized plants and birds; a situation well known from hummingbirds and specialized plant communities of the New World. Additionally, the herbaceous habits of Impatiens species, the frequent adaptations to pollination by hovering birds, and the habitat preference for understory in tropical forests or epiphytic growth, resemble the highly specialized Neotropical plants. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 127–133.     

Browridge development in cercopithecidae: A test of two models

Theoretical discussions of primate browridge formation have resulted in several interpretations of its form and function. Lateral radiographs of adult Old World monkeys, representing most cercopithecine and colobine genera, were examined to address whether both biomechanical and spatial factors influence the development of a supraorbital torus. A linear measurement of browridge size was compared with a series of measures related to each model. Partial correlations were used to ascertain the relative independence of biomechanical (model I or II) and spatial effects upon torus formation. Allometric (size-related) shape changes were evaluated with log-linear bivariate regression analysis; subfamily differences in scaling patterns, with an analysis of covariance. When spatial and biomechanical (I or II) factors were both significantly related to brow size, additive and interactive multiple regression models were used to further assess the manner by which each set mutually affects variation in browridge dimensions. Correlation analyses were repeated with size-corrected antilogged residuals to eliminate a potentially spurious effect of skull size. Old World monkeys provide support of the spatial model. Also of interest is that skull size emerges as a primary influence on torus formation. Several alternative explanations are also put forward to account for browridge development in each subfamily.     

Sexual selection and the evolution of secondary sexual traits: sex comb evolution in Drosophila

Sexual selection can drive rapid evolutionary change in reproductive behaviour, morphology and physiology. This often leads to the evolution of sexual dimorphism, and continued exaggerated expression of dimorphic sexual characteristics, although a variety of other alternative selection scenarios exist. Here, we examined the evolutionary significance of a rapidly evolving, sexually dimorphic trait, sex comb tooth number, in two Drosophila species. The presence of the sex comb in both D. melanogaster and D. pseudoobscura is known to be positively related to mating success, although little is yet known about the sexually selected benefits of sex comb structure. In this study, we used experimental evolution to test the idea that enhancing or eliminating sexual selection would lead to variation in sex comb tooth number. However, the results showed no effect of either enforced monogamy or elevated promiscuity on this trait. We discuss several hypotheses to explain the lack of divergence, focussing on sexually antagonistic coevolution, stabilizing selection via species recognition and nonlinear selection. We discuss how these are important, but relatively ignored, alternatives in understanding the evolution of rapidly evolving sexually dimorphic traits.