Evolutionary origin of the amnioserosa in cyclorrhaphan flies correlates with spatial and temporal expression changes of
            <i>zen</i>

Rafiqi, Ab. Matteen; Lemke, Steffen; Ferguson, Sean; Stauber, Michael; Schmidt‐Ott, Urs

doi:10.1073/pnas.0709145105

Cited by 77 publications

(127 citation statements)

References 39 publications

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“…If syrphids are closer relatives to higher flies than phorids, as our molecular tree denotes, it indicates either parallel evolution in Megaselia and schizophorans or a reversal to an ancestral mode of development in Episyrphus. Fur-thermore, a paraphyletic relationship of phorids and syrphids would support the hypothesis that their shared special mode of extraembryonic development (dorsal amnion closure) (26) evolved in the stem lineage of Cyclorrhapha and preceded the origin of the schizophoran amnioserosa.…”

Section: Resultsmentioning

confidence: 71%

Episodic radiations in the fly tree of life

Wiegmann¹,

Trautwein²,

Winkler³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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778

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Flies are one of four superradiations of insects (along with beetles, wasps, and moths) that account for the majority of animal life on Earth. Diptera includes species known for their ubiquity (Musca domestica house fly), their role as pests (Anopheles gambiae malaria mosquito), and their value as model organisms across the biological sciences (Drosophila melanogaster). A resolved phylogeny for flies provides a framework for genomic, developmental, and evolutionary studies by facilitating comparisons across model organisms, yet recent research has suggested that fly relationships have been obscured by multiple episodes of rapid diversification. We provide a phylogenomic estimate of fly relationships based on molecules and morphology from 149 of 157 families, including 30 kb from 14 nuclear loci and complete mitochondrial genomes combined with 371 morphological characters. Multiple analyses show support for traditional groups (Brachycera, Cyclorrhapha, and Schizophora) and corroborate contentious findings, such as the anomalous Deuterophlebiidae as the sister group to all remaining Diptera. Our findings reveal that the closest relatives of the Drosophilidae are highly modified parasites (including the wingless Braulidae) of bees and other insects. Furthermore, we use micro-RNAs to resolve a node with implications for the evolution of embryonic development in Diptera. We demonstrate that flies experienced three episodes of rapid radiation-lower Diptera (220 Ma), lower Brachycera (180 Ma), and Schizophora (65 Ma)-and a number of life history transitions to hematophagy, phytophagy, and parasitism in the history of fly evolution over 260 million y.T he history of life is often portrayed as an ongoing series of evolutionary bursts, with each representing the origin and diversification of unique life forms with different and ecologically significant adaptations. Although the radiations of some groups, such as cichlid fishes of the lakes of East Africa or Darwin's finches, are well documented (1), the big radiations that account for most of the diversity of life on Earth have been more challenging to explore. To understand these radiations, we must resolve the relationships among major taxa, date the origin of these lineages (many of them ancient), and then explicitly consider whether the diversification events are really pulse-like adaptive radiations or, more simply, the result of nonadaptive, or even random, neutral processes.Although the paradigm of adaptive radiation has been applied to every level of biological classification, the large-scale macroevolutionary pattern expected from ancient repeated episodes of adaptive radiation is unclear. It has been predicted that at this scale, ecologically driven diversification may result in (i) significant variation in clade size, uncorrelated to the age of the clade (2), and (ii) shifts in average diversification rate coincident with major shifts in morphology, life history, or ecology (3). Another macroevolutionary prediction of repeated adaptive radiation is the widespre...

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Section: Resultsmentioning

confidence: 71%

Episodic radiations in the fly tree of life

Wiegmann¹,

Trautwein²,

Winkler³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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778

1,018

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“…For single-color in situ hybridization, M. abdita embryos were collected, heat fixed and hybridized as described (Rafiqi et al, 2008;Rafiqi et al, 2011). Antisense RNA probes were prepared from the linearized pCRII-TOPO plasmids of the PCR clones and labeled with digoxigenin or FITC as described (Tautz and Pfeifle, 1989;Kosman et al, 2004).…”

Section: In Situ Hybridization Immunohistochemistry Rnai and Mrna Imentioning

confidence: 99%

“…This tissue is specified along the dorsal midline of the blastoderm and closes the dorsal side of the germband. In non-schizophoran dipterans, dorsal blastoderm folds over the gastrulating embryo and differentiates into two tissues: a cuticle-secreting serosa underneath the eggshell and an amnion that either lines the ventral side or closes the dorsal side of the germband (Goltsev et al, 2007;Rafiqi et al, 2008;Goltsev et al, 2009). Dorsal patterning of the dipteran embryo must have changed with the evolutionary transition from two extra-embryonic tissue types to one, but whether the transition involved altered BMP activity or genetic changes downstream or independent of this signaling pathway is unknown.…”

Section: Introductionmentioning

confidence: 99%

BMP-dependent serosa and amnion specification in the scuttle fly Megaselia abdita

et al. 2012

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SUMMARYBone morphogenetic protein (BMP) signaling is an essential factor in dorsoventral patterning of animal embryos but how BMP signaling evolved with fundamental changes in dorsoventral tissue differentiation is unclear. Flies experienced an evolutionary reduction of extra-embryonic tissue types from two (amniotic and serosal tissue) to one (amnionserosal tissue). BMP-dependent amnioserosa specification has been studied in Drosophila melanogaster. However, the mechanisms of serosal and amniotic tissue specification in less diverged flies remain unknown. To better understand potential evolutionary links between BMP signaling and extra-embryonic tissue specification, we examined the activity profile and function of BMP signaling in serosa and amnion patterning of the scuttle fly Megaselia abdita (Phoridae) and compared the BMP activity profiles between M. abdita and D. melanogaster. In blastoderm embryos of both species, BMP activity peaked at the dorsal midline. However, at the beginning of gastrulation, peak BMP activity in M. abdita shifted towards prospective amnion tissue. This transition correlated with the first signs of amnion differentiation laterally adjacent to the serosa anlage. Marker-assisted analysis of six BMP signaling components (dpp, gbb, scw, tkv, sax, sog) by RNA interference revealed that both serosa and amnion specification of M. abdita are dependent on BMP activity. Conversely, BMP gain-of-function experiments caused sharpened expression boundaries of extra-embryonic target genes indicative of positive feedback. We propose that changes in the BMP activity profile at the beginning of gastrulation might have contributed to the reduction of extra-embryonic tissue types during the radiation of cyclorrhaphan flies.

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“…The PCR product was digested with NcoI and SalI and cloned into pSP35, and capped mRNA was synthesized as described (Lemke and Schmidt-Ott, 2009). Injection and fixation of embryos was carried out as described (Lemke and Schmidt-Ott, 2009;Rafiqi et al, 2008).…”

Section: Cloning Proceduresmentioning

confidence: 99%

“…Episyrphus belongs to the sister taxon of higher cyclorrhaphan flies (Schizophora, including Drosophila) (Grimaldi and Engel, 2005;Lemke and Schmidt-Ott, 2009;Yeates and Wiegmann, 2005) and is currently one of the most 'basal' dipteran species amenable to functional genetic studies in early embryos (Lemke and Schmidt-Ott, 2009;Rafiqi et al, 2008). Like Drosophila, Episyrphus specifies segments simultaneously prior to gastrulation (long-germ development) (Bullock et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Maternal activation of gap genes in the hover flyEpisyrphus

et al. 2010

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The metameric organization of the insect body plan is initiated with the activation of gap genes, a set of transcription-factor-encoding genes that are zygotically expressed in broad and partially overlapping domains along the anteroposterior (AP) axis of the early embryo. The spatial pattern of gap gene expression domains along the AP axis is generally conserved, but the maternal genes that regulate their expression are not. Building on the comprehensive knowledge of maternal gap gene activation in Drosophila, we used loss- and gain-of-function experiments in the hover fly Episyrphus balteatus (Syrphidae) to address the question of how the maternal regulation of gap genes evolved. We find that, in Episyrphus, a highly diverged bicoid ortholog is solely responsible for the AP polarity of the embryo. Episyrphus bicoid represses anterior zygotic expression of caudal and activates the anterior and central gap genes orthodenticle, hunchback and Krüppel. In bicoid-deficient Episyrphus embryos, nanos is insufficient to generate morphological asymmetry along the AP axis. Furthermore, we find that torso transiently regulates anterior repression of caudal and is required for the activation of orthodenticle, whereas all posterior gap gene domains of knirps, giant, hunchback, tailless and huckebein depend on caudal. We conclude that all maternal coordinate genes have altered their specific functions during the radiation of higher flies (Cyclorrhapha).

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Evolutionary origin of the amnioserosa in cyclorrhaphan flies correlates with spatial and temporal expression changes of zen

Cited by 77 publications

References 39 publications

Episodic radiations in the fly tree of life

Episodic radiations in the fly tree of life

BMP-dependent serosa and amnion specification in the scuttle fly Megaselia abdita

Maternal activation of gap genes in the hover flyEpisyrphus

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