Staff Profiles

Biological Sciences BSc (Hons) 

Animal Biology and Conservation BSc (Hons) 

MBiol Biology

Eco Evo Devo Postgraduate Summer School

Modules taught

Undergraduate

Level 4 

• BIOL4004: The Practicing Scientist
• BIOL5013: Research Methods for Biology and Environmental Sciences 

Level 5 

• BIOL5014: Molecular Biology (module leader)
• BIOL5015: Genetics (module leader)

Level 6 

• BIOL 6011: Advanced Genetics and Genomics
• BIOL6012: Animal Neurobiology and Behaviour (module leader)
• BIOL 6005: Evolution and Animal Development
• BIOS6010: Project
• BIOL6009: Independent Study in Life Sciences 

Supervision

Master students

Evelyne Mann (Vetmed Uni, Vienna, 2009)

Victoria Steinmann (Vetmed Uni, Vienna, 2011)

PhD students

Luis Baudouin Gonzalez (second supervisor, Oxford Brookes University, ongoing)

Abigail Bailey (second supervisor, Oxford Brookes University, ongoing)

Anna Schönauer (second supervisor, Oxford Brookes University, 2013-2016)

Christian Bonatto Paese (second supervisor, Oxford Brookes University, 2015-2018)

Michaela Holzem (second supervisor, Oxford Brookes University, 2015-2019)

Joanna Hagen (main supervisor, Oxford Brookes University, 2015-2019)

PostDocs

Dr. Rachel Wade (co-supervisor, main supervisor: Professor Tim Shreeve)

Phenotypic evolution and adaptation

We are an Evolutionary Biology Group with a particular focus on Molecular evolution, Population Genetics and Evolutionary Developmental Biology.

Currently, our research aims to provide a better understanding of the genetic basis of complex quantitative traits and the evolutionary processes responsible for their evolution.

Research grants and awards

September 2015- September 2018. Nigel Groome Research Studentship to sponsor Joanna Hagen PhD work.

January 2015- December 2017. ‘Characterising the genetic architecture and fitness effects of rapid morphological diversification.’ NERC. £417,670. (as Researcher Co-investigator)

Further information

Journal articles

• Hagen JFD, Mendes CC, Blogg A, Payne A, Tanaka KM, Gaspar P, Jimenez JF, Kittelmann M, McGregor AP, Nunes MDS, 'tartan underlies the evolution of Drosophila male genital morphology'
  Proceedings of the National Academy of Sciences (2019)
  ISSN: 0027-8424 eISSN: 1091-6490
  Abstract

  Male genital structures are among the most rapidly evolving morphological traits and are often the only features that can distinguish closely related species. This process is thought to be driven by sexual selection and may reinforce species separation. However, while the genetic bases of many phenotypic differences have been identified, we still lack knowledge about the genes underlying evolutionary differences in male genital organs and organ size more generally. The claspers (surstyli) are periphallic structures that play an important role in copulation in insects. Here, we show that divergence in clasper size and bristle number between Drosophila mauritiana and Drosophila simulans is caused by evolutionary changes in tartan (trn), which encodes a transmembrane leucine-rich repeat domain protein that mediates cell–cell interactions and affinity. There are no fixed amino acid differences in trn between D. mauritiana and D. simulans, but differences in the expression of this gene in developing genitalia suggest that cis-regulatory changes in trn underlie the evolution of clasper morphology in these species. Finally, analyses of reciprocal hemizygotes that are genetically identical, except for the species from which the functional allele of trn originates, determined that the trn allele of D. mauritiana specifies larger claspers with more bristles than the allele of D. simulans. Therefore, we have identified a gene underlying evolutionary change in the size of a male genital organ, which will help to better understand not only the rapid diversification of these structures, but also the regulation and evolution of organ size more broadly.
  

  Website 
• Rice G, David JR, Kamimura Y, Masly JP, Mcgregor AP, Nagy O, Noselli S, Nunes MDS, O'Grady P, Sánchez-Herrero E, Siegal ML, Toda MJ, Rebeiz M, Courtier-Orgogozo V, Yassin A., 'A standardized nomenclature and atlas of the male terminalia of Drosophila melanogaster'
  Fly (2019)
  ISSN: 1933-6934 eISSN: 1933-6942
  Abstract

  Animal terminalia represent some of the most diverse and rapidly evolving structures in the animal kingdom, and for this reason have been a mainstay in the taxonomic description of species. The terminalia of Drosophila melanogaster, with its wide range of experimental tools, have recently become the focus of increased interest in the fields of development, evolution, and behavior. However, studies from different disciplines have often used discrepant terminologies for the same anatomical structures. Consequently, the terminology of genital parts has become a barrier to integrating results from different fields, rendering it difficult to determine what parts are being referenced. We formed a consortium of researchers studying the genitalia of D. melanogaster to help establish a set of naming conventions. Here, we present a detailed visual anatomy of male genital parts, including a list of synonymous terms, and suggest practices to avoid confusion when referring to anatomical parts in future studies. The goal of this effort is to facilitate interdisciplinary communication and help newcomers orient themselves within the exciting field of Drosophila genitalia.
  

  Website 
• Kittelmann S, Buffry AD, Franke FA, Almudi I, Yoth M, Sabaris G, Couso JP, Nunes MDS, Frankel N, Gómez-Skarmeta JL, Pueyo-Marques J, Arif S, McGregor AP, 'Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution'
  PLoS Genetics 14 (5) (2018)
  ISSN: 1553-7390 eISSN: 1553-7404
  Abstract Convergent phenotypic evolution is often caused by recurrent changes at particular nodes in the underlying gene regulatory networks (GRNs). The genes at such evolutionary ‘hotspots’ are thought to maximally affect the phenotype with minimal pleiotropic consequences. This has led to the suggestion that if a GRN is understood in sufficient detail, the path of evolution may be predictable. The repeated evolutionary loss of larval trichomes among Drosophila species is caused by the loss of shavenbaby (svb) expression. svb is also required for development of leg trichomes, but the evolutionary gain of trichomes in the ‘naked valley’ on T2 femurs in Drosophila melanogaster is caused by the loss of microRNA-92a (miR-92a) expression rather than changes in svb. We compared the expression and function of components between the larval and leg trichome GRNs to investigate why the genetic basis of trichome pattern evolution differs in these developmental contexts. We found key differences between the two networks in both the genes employed, and in the regulation and function of common genes. These differences in the GRNs reveal why mutations in svb are unlikely to contribute to leg trichome evolution and how instead miR-92a represents the key evolutionary switch in this context. Our work shows that variability in GRNs across different developmental contexts, as well as whether a morphological feature is lost versus gained, influence the nodes at which a GRN evolves to cause morphological change. Therefore, our findings have important implications for understanding the pathways and predictability of evolution.Website 
• Tanaka KM, Hopfen C, Herbert MR, Schlotterer C, Stern DL, Masly JP, McGregor AP, Nunes MD, 'Genetic architecture and functional characterization of genes underlying the rapid diversification of male external genitalia between Drosophila simulans and Drosophila mauritiana'
  Genetics 200 (1) (2015) pp.357-369
  ISSN: 0016-6731
  Abstract
  Male sexual characters are often among the first traits to diverge between closely related species and identifying the genetic basis of such changes can contribute to our understanding of their evolutionary history. However, little is known about the genetic architecture or the specific genes underlying the evolution of male genitalia. The morphology of the claspers, posterior lobes, and anal plates exhibit striking differences between Drosophila mauritiana and D. simulans. Using QTL and introgression-based high-resolution mapping, we identified several small regions on chromosome arms 3L and 3R that contribute to differences in these traits. However, we found that the loci underlying the
  evolution of clasper differences between these two species are independent from those that contribute to posterior lobe and anal plate divergence. Furthermore, while most of the loci affect each trait in the same direction and act additively, we also found evidence for epistasis between loci for clasper bristle number. In addition, we conducted an RNAi screen in D. melanogaster to investigate if positional and expression candidate genes located on chromosome 3L, are also involved in genital development. We found that six of these genes, including components of Wnt signaling and male-specific lethal 3 (msl3), regulate the development of genital traits consistent with the effects of the introgressed regions where they are located and that thus represent promising candidate genes for the evolution these traits.
  Website 
• Hilbrant M, Almudi I, Leite DJ, Kuncheria L, Posnien N, Nunes MDS, McGregor AP, 'Sexual dimorphism and natural variation within and among species in the Drosophila retinal mosaic'
  BMC Evolutionary Biology 14 (2014) pp.240-
  ISSN: 1471-2148
  Abstract
  Background
   
  Insect compound eyes are composed of ommatidia, which contain photoreceptor cells that are sensitive to different wavelengths of light defined by the specific rhodopsin proteins that they express. The fruit fly Drosophila melanogaster has several different ommatidium types that can be localised to specific retinal regions, such as the dorsal rim area (DRA), or distributed stochastically in a mosaic across the retina, like the ‘pale’ and ‘yellow’ types. Variation in these ommatidia patterns very likely has important implications for the vision of insects and could underlie behavioural and environmental adaptations. However, despite the detailed understanding of ommatidia specification in D. melanogaster, the extent to which the frequency and distribution of the different ommatidium types vary between sexes, strains and species of Drosophila is not known.
   
  Results
   
  We investigated the frequency and distribution of ommatidium types based on rhodopsin protein expression, and the expression levels of rhodopsin transcripts in the eyes of both sexes of different strains of D. melanogaster, D. simulans and D. mauritiana. We found that while the number of DRA ommatidia was invariant, Rh3 expressing ommatidia were more frequent in the larger eyes of females compared to the males of all species analysed. The frequency and distribution of ommatidium types also differed between strains and species. The D. simulans strain ZOM4 has the highest frequency of Rh3 expressing ommatidia, which is associated with a non-stochastic patch of pale and odd-coupled ommatidia in the dorsal-posterior of their eyes.
   
  Conclusions
   
  Our results show that there is striking variation in the frequency and distribution of ommatidium types between sexes, strains and species of Drosophila. This suggests that evolutionary changes in the underlying regulatory mechanisms can alter the distribution of ommatidium types to promote or restrict their expression in specific regions of the eye within and between species, and that this could cause differences in vision among these flies.
  Website 
• Nunes MDS, Arif S, Schlotterer C, McGregor AP, 'A perspective on micro-evo-devo: progress and potential'
  Genetics 195 (3) (2013) pp.625-634
  ISSN: 0016-6731
  Abstract The term micro-evo-devo refers to the combined study of the genetic and developmental bases of natural variation in populations and the evolutionary forces that have shaped this variation. It thus represents a synthesis of the fields of evolutionary developmental biology and population genetics. As has been pointed out by several others, this synthesis can provide insights into the evolution of organismal form and function that have not been possible within these individual disciplines separately. Despite a number of important successes in micro-evo-devo, however, it appears that evo devo and population genetics remain largely separate spheres of research, limiting their ability to address evolutionary questions. This also risks pushing contemporary evo devo to the fringes of evolutionary biology because it does not describe the causative molecular changes underlying evolution or the evolutionary forces involved. Here we reemphasize the theoretical and practical importance of micro-evo-devo as a strategy for understanding phenotypic evolution, review the key recent insights that it has provided, and present a perspective on both the potential and the remaining challenges of this exciting interdisciplinary field.Website 
• Nunes MDS, Dolezal M, Schlotterer C, 'Extensive paternal mtDNA leakage in natural populations of Drosophila melanogaster'
  MOLECULAR ECOLOGY 22 (8) (2013) pp.2106-2117
  ISSN: 0962-1083
  Abstract Strict maternal inheritance is considered a hallmark of animal mtDNA. Although recent reports suggest that paternal leakage occurs in a broad range of species, it is still considered an exceptionally rare event. To evaluate the impact of paternal leakage on the evolution of mtDNA, it is essential to reliably estimate the frequency of paternal leakage in natural populations. Using allele-specific real-time quantitative PCR (RT-qPCR), we show that heteroplasmy is common in natural populations with at least 14% of the individuals carrying multiple mitochondrial haplotypes. However, the average frequency of the minor mtDNA haplotype is low (0.8%), which suggests that this pervasive heteroplasmy has not been noticed before due to a lack of power in sequencing surveys. Based on the distribution of mtDNA haplotypes in the offspring of heteroplasmic mothers, we found no evidence for strong selection against one of the haplotypes. We estimated that the rate of paternal leakage is 6% and that at least 100 generations are required for complete sorting of mtDNA haplotypes. Despite the high proportion of heteroplasmic individuals in natural populations, we found no evidence for recombination between mtDNA molecules, suggesting that either recombination is rare or recombinant haplotypes are counter-selected. Our results indicate that evolutionary studies using mtDNA as a marker might be biased by paternal leakage in this species.Website 
• Arif S, Murat S, Almudi I, Nunes M, Bortolamiol-Becet D, McGregor N, Currie J, Hughes H, Ronshaugen M, Sucena E, Lai E, Schlottere C, McGregor A, 'Evolution of mir-92a underlies natural morphological variation in Drosophila melanogaster'
  Current Biology 23 (6) (2013) pp.523-528
  ISSN: 0960-9822
  Abstract

  Identifying the genetic mechanisms underlying phenotypic change is essential to understanding how gene regulatory networks and ultimately the genotype-to-phenotype map evolve. It is recognized that microRNAs (miRNAs) have the potential to facilitate evolutionary change [1, 2and3]; however, there are no known examples of natural morphological variation caused by evolutionary changes in miRNA expression. Therefore, the contribution of miRNAs to evolutionary change remains unknown [1and4]. Drosophila melanogaster subgroup species display a portion of trichome-free cuticle on the femur of the second leg called the "naked valley." It was previously shown that Ultrabithorax (Ubx) is involved in naked valley variation between D.melanogaster and D.simulans [ 5and6]. However, naked valley size also varies among populations of D.melanogaster, ranging from 1,000 up to 30,000μm2. We investigated the genetic basis of intraspecific differences in the naked valley in D.melanogaster and found that neither Ubx nor shavenbaby (svb) [ 7and8] contributes to this morphological difference. Instead, we show that changes in mir-92a expression underlie the evolution of naked valley size in D.melanogaster through repression of shavenoid (sha) [9]. Therefore, our results reveala novel mechanism for morphological evolution and suggest that modulation of the expression of miRNAs potentially plays a prominent role in generating organismal diversity.

  Website 
• Arif S, Hilbrant M, Hopfen C, Almudi I, Nunes MDS, Posnien N, Kuncheria L, Tanaka K, Mitteroecker P, Schlotterer C, McGregor AP, 'Genetic and Developmental Analysis of Differences in Eye and Face Morphology Between Drosophila Simulans and Drosophila Mauritiana'
  Evolution and Development 15 (2013) pp.257-267
  ISSN: 1520-541X eISSN: 1525-142X
  Abstract

  Eye and head morphology vary considerably among insects and even between closely related species of Drosophila. Species of the D. melanogaster subgroup, and other Drosophila species, exhibit a negative correlation between eye size and face width (FW); for example, D. mauritiana generally has bigger eyes composed of larger ommatidia and conversely a narrower face than its sibling species. To better understand the evolution of eye and head morphology, we investigated the genetic and developmental basis of differences in eye size and FW between male D. mauritiana and D. simulans. QTL mapping of eye size and FW showed that the major loci responsible for the interspecific variation in these traits are localized to different genomic regions. Introgression of the largest effect QTL underlying the difference in eye size resulted in flies with larger eyes but no significant difference in FW. Moreover, introgression of a QTL region on the third chromosome that contributes to the FW difference between these species affected FW, but not eye size. We also observed that this difference in FW is detectable earlier in the development of the eye-antennal disc than the difference in the size of the retinal field. Our results suggest that different loci that act at different developmental stages underlie changes in eye size and FW. Therefore, while there is a negative correlation between these traits in Drosophila, we show genetically that they also have the potential to evolve independently and this may help to explain the evolution of these traits in other insects.

  Website 
• Posnien N, Hopfen C, Hilbrant M, Ramos-Womack M, Murat S, Schonauer A, Herbert S, Nunes M, Arif S, Breuker C J, Schlotterer C, Mitteroecker P, McGregor AP, 'Evolution of eye morphology and rhodopsin expression in the Drosophila melanogaster species subgroup.'
  PLoS ONE 7 (5) (2012) pp.e37346-
  ISSN: 1932-6203
  Abstract

  A striking diversity of compound eye size and shape has evolved among insects. The number of ommatidia and their size are major determinants of the visual sensitivity and acuity of the compound eye. Each ommatidium is composed of eight photoreceptor cells that facilitate the discrimination of different colours via the expression of various light sensitive Rhodopsin proteins. It follows that variation in eye size, shape, and opsin composition is likely to directly influence vision. We analyzed variation in these three traits in D. melanogaster, D. simulans and D. mauritiana. We show that D. mauritiana generally has larger eyes than its sibling species, which is due to a combination of larger ommatidia and more ommatidia. In addition, intra- and inter-specific differences in eye size among D. simulans and D. melanogaster strains are mainly caused by variation in ommatidia number. By applying a geometric morphometrics approach to assess whether the formation of larger eyes influences other parts of the head capsule, we found that an increase in eye size is associated with a reduction in the adjacent face cuticle. Our shape analysis also demonstrates that D. mauritiana eyes are specifically enlarged in the dorsal region. Intriguingly, this dorsal enlargement is associated with enhanced expression of rhodopsin 3 in D. mauritiana. In summary, our data suggests that the morphology and functional properties of the compound eyes vary considerably within and among these closely related Drosophila species and may be part of coordinated morphological changes affecting the head capsule.

  Website 
• Nunes M D S, Orozco-Ter Wengel P, Kreissl M, Schlotterer C, 'Multiple hybridization events between Drosophila simulans and Drosophila mauritiana are supported by mtDNA introgression'
  Molecular Ecology 19 (21) (2010) pp.4695-4707
  ISSN: 0962-1083 eISSN: 1365-294X
  Abstract

  The study of speciation has advanced considerably in the last decades because of the increased application of molecular tools. In particular, the quantification of gene flow between recently diverged species could be addressed. Drosophila simulans and Drosophila mauritiana diverged, probably allopatrically, from a common ancestor approximately 250000years ago. However, these species share one mitochondrial DNA (mtDNA) haplotype indicative of a recent episode of introgression. To study the extent of gene flow between these species, we took advantage of a large sample of D.mauritiana and employed a range of different markers, i.e. nuclear and mitochondrial sequences, and microsatellites. This allowed us to detect two new mtDNA haplotypes (MAU3 and MAU4). These haplotypes diverged quite recently from haplotypes of the siII group present in cosmopolitan populations of D.simulans. The mean divergence time of the most diverged haplotype (MAU4) is approximately 127000years, which is more than 100000years before the assumed speciation time. Interestingly, we also found some evidence for gene flow at the nuclear level because an excess of putatively neutral loci shows significantly reduced differentiation between D.simulans and D.mauritiana. Our results suggest that these species are exchanging genes more frequently than previously thought.

  Website 
• Nunes M D S, Nolte V, Scholotterer C, 'Nonrandom Wolbachia infection status of Drosophila melanogaster strains with different mtDNA haplotypes'
  Molecular Biology and Evolution 25 (11) (2008) pp.2493-2498
  ISSN: 0737-4038 eISSN: 1537-1719
  Abstract Wolbachia are maternally inherited bacteria, which typically spread in the host population by inducing cytoplasmic incompatibility (CI). In Drosophila melanogaster, Wolbachia is quite common but CI is variable, with most of the studies reporting low levels of CI. Surveying mitochondrial DNA (mtDNA) variation and infection status in a worldwide D. melanogaster collection, we found that the Wolbachia infection was not randomly distributed among flies with different mtDNA haplotypes. This preferential infection of some mtDNA haplotypes could be caused by a recent spread of mtDNA haplotypes associated with the infection. The comparison of contemporary D. melanogaster samples with lines collected more than 50 years ago shows that indeed one haplotype with a high incidence of Wolbachia infection has increased in frequency. Consistent with this observation, we found that the acquisition of a Wolbachia infection in a population from Crete was accompanied with an almost complete mtDNA replacement, with the Wolbachia-associated haplotype becoming abundant. Although it is difficult to identify the evolutionary forces causing the global increase of wMel, the parallel sweep of Wolbachia and an mtDNA haplotype suggests a fitness advantage of the Wolbachia infection.Website 
• Nunes, M D S Neumeier H, and Schlotterer C, 'Contrasting patterns of natural variation in global Drosophila melanogaster populations'
  Molecular Ecology 17 (20) (2008) pp.4470-4479
  ISSN: 0962-1083 eISSN: 1365-294X
  Abstract Despite the popularity of Drosophila melanogaster in functional and evolutionary genetics, the global pattern of natural variation has not yet been comprehensively described in this species. For the first time, we report a combined survey using neutral microsatellites and mitochondrial sequence variation jointly. Thirty-five populations originating from five continents were compared. In agreement with previous microsatellite studies, sub-Saharan African populations were the most variable ones. Consistent with previous reports of a single ‘out of Africa' habitat expansion, we found that non-African populations contained a subset of the African alleles. The pattern of variation detected for the mitochondrial sequences differed substantially. The most divergent haplotypes were detected in the Mediterranean region while Africa harboured most haplotypes, which were all closely related. In the light of the well-established African origin of D. melanogaster, our results cast severe doubts about the suitability of mtDNA for biogeographic inference in this model organism.Website 
• Nunes MDS, Santos RAM, Ferreira SM, Vieira J, Vieira CP, 'Variability patterns and positively selected sites at the gametophytic self-incompatibility pollen SFB gene in a wild self-incompatible Prunus spinosa (Rosaceae) population'
  NEW PHYTOLOGIST 172 (2006) pp.577-587
  ISSN: 0028-646X
  Abstract None of the models is compatible with the variability patterns found in the SFB and the S-haplotype data.Website 

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