Assessing Differences in Sperm Competitive Ability in <em>Drosophila</em>

Competition among conspecific males for fertilizing the ova is one of the mechanisms of sexual selection, i.e. selection that operates on maximizing the ...

University of California, Irvine

Many proteins are used repeatedly in development, but usually the function of the protein is similar in the different contexts. Here we report that the classical Drosophila melanogaster locus tan encodes a novel enzyme required for two very different cellular functions: hydrolysis of N-beta-alanyl dopamine (NBAD) to dopamine during cuticular melanization, and hydrolysis of carcinine to histamine in the metabolism of photoreceptor neurotransmitter. We characterized two tan-like P-element insertions that failed to complement classical tan mutations. Both are inserted in the 5' untranslated region of the previously uncharacterized gene CG12120, a putative homolog of fungal isopenicillin-N N-acyltransferase (EC 2.3.1.164). Both P insertions showed abnormally low transcription of the CG12120 mRNA. Ectopic CG12120 expression rescued tan mutant pigmentation phenotypes and caused the production of striking black melanin patterns. Electroretinogram and head histamine assays indicated that CG12120 is required for hydrolysis of carcinine to histamine, which is required for histaminergic neurotransmission. Recombinant CG12120 protein efficiently hydrolyzed both NBAD to dopamine and carcinine to histamine. We conclude that D. melanogaster CG12120 corresponds to tan. This is, to our knowledge, the first molecular genetic characterization of NBAD hydrolase and carcinine hydrolase activity in any organism and is central to the understanding of pigmentation and photoreceptor function.

Drosophila tan encodes a novel hydrolase required in pigmentation and vision.

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The independent evolution of morphological similarities is widespread. For simple traits, such as overall body colour, repeated transitions by means of mutations in the same gene may be common. However, for more complex traits, the possible genetic paths may be more numerous; the molecular mechanisms underlying their independent origins and the extent to which they are constrained to follow certain genetic paths are largely unknown. Here we show that a male wing pigmentation pattern involved in courtship display has been gained and lost multiple times in a Drosophila clade. Each of the cases we have analysed (two gains and two losses) involved regulatory changes at the pleiotropic pigmentation gene yellow. Losses involved the parallel inactivation of the same cis-regulatory element (CRE), with changes at a few nucleotides sufficient to account for the functional divergence of one element between two sibling species. Surprisingly, two independent gains of wing spots resulted from the co-option of distinct ancestral CREs. These results demonstrate how the functional diversification of the modular CREs of pleiotropic genes contributes to evolutionary novelty and the independent evolution of morphological similarities.

Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene.

L&#x26;#39;&#xE9;volution ind&#xE9;pendante des similitudes morphologiques est tr&#xE8;s r&#xE9;pandue. Pour de simples traits, comme la couleur g&#xE9;n&#xE9;rale du corps, r&#xE9;p&#xE9;t&#xE9; transitions par des moyens de mutations dans le g&#xE8;ne m&#xEA;me peut-&#xEA;tre commun. Toutefois, pour les caract&#xE8;res plus complexes, les chemins possibles g&#xE9;n&#xE9;tiques peuvent &#xEA;tre plus nombreux, les m&#xE9;canismes mol&#xE9;culaires qui sous-tendent leurs origines ind&#xE9;pendantes et la mesure dans laquelle ils sont contraints de suivre certaines voies g&#xE9;n&#xE9;tiques sont largement inconnues. Ici, nous montrons qu&#x26;#39;un mod&#xE8;le aile masculine impliqu&#xE9;s dans la pigmentation parade nuptiale a &#xE9;t&#xE9; gagn&#xE9; et perdu plusieurs fois dans un clade drosophile. Chacun des cas que nous avons analys&#xE9;s (deux gains et deux revers) impliqu&#xE9; des changements r&#xE9;glementaires au jaune g&#xE8;ne de pigmentation pl&#xE9;iotrope. Pertes impliqu&#xE9;s l&#x26;#39;inactivation parall&#xE8;le de la m&#xEA;me cis-r&#xE9;gulation &#xE9;l&#xE9;ment (CRE), avec des changements de quelques nucl&#xE9;otides suffisantes pour rendre compte de l&#x26;#39;&#xE9;cart d&#x26;#39;un &#xE9;l&#xE9;ment fonctionnel entre deux esp&#xE8;ces apparent&#xE9;es. &#xC9;tonnamment, deux gains ind&#xE9;pendants de taches aile r&#xE9;sulte de la cooptation de diff&#xE9;rentes CRE ancestrales. Ces r&#xE9;sultats montrent comment la diversification fonctionnelle des g&#xE8;nes de CRE modulaires pl&#xE9;iotropiques contribue &#xE0; la nouveaut&#xE9; de l&#x26;#39;&#xE9;volution et l&#x26;#39;&#xE9;volution ind&#xE9;pendante des similitudes morphologiques.

R&#xE9;p&#xE9;t&#xE9;e &#xE9;volution morphologique Gr&#xE2;ce cis-r&#xE9;gulatrices des modifications dans un g&#xE8;ne pl&#xE9;iotropique

Die unabh&auml;ngige Entwicklung der morphologischen &Auml;hnlichkeiten ist weit verbreitet. F&uuml;r einfache Merkmale, wie allgemeine Wagenfarbe m&ouml;glicherweise wiederholte &Uuml;berg&auml;nge durch Mutationen im gleichen Gen gemeinsame. F&uuml;r komplexere Merkmale, k&ouml;nnen jedoch die m&ouml;glichen genetischen Pfade zahlreicher sein; die molekularen Mechanismen ihre unabh&auml;ngige Herkunft und das Ausma&szlig;, zu dem sie beschr&auml;nkt sind, bestimmte genetische Wege zu gehen, sind weitgehend unbekannt. Hier zeigen wir, dass eine m&auml;nnlicher Fl&uuml;gel Pigmentierung Muster beteiligt Freiendemonstration gewonnen und mehrfach in eine Drosophila-Klade verloren wurde. Jeden der F&auml;lle haben wir analysiert (zwei Gewinne und zwei Niederlagen) beteiligt regulatorische &Auml;nderungen bei den pleiotropen Pigmentierung gen gelb. Verluste beteiligt die parallele Inaktivierung des gleichen Cis-regulatorische Elements (CRE), mit &Auml;nderungen auf wenige Nukleotide ausreichen, um die funktionalen Divergenz der ein Element zwischen zwei gleichgeordneten Arten zu ber&uuml;cksichtigen. &Uuml;berraschenderweise ergab sich zwei unabh&auml;ngige Gewinne Fl&uuml;gel Spots aus der Kooptation unterschiedliche Vorfahren Cres Diese Ergebnisse zeigen, wie die funktionale Diversifizierung der modularen Cres pleiotropen Gene zur evolution&auml;ren Neuheit und die unabh&auml;ngige Entwicklung der morphologischen &Auml;hnlichkeiten beitr&auml;gt.

Wiederholte morphologische Entwicklung durch Cis-regulatorischen &Auml;nderungen in einem pleiotropen gen.

L&#39;evoluzione indipendente di somiglianze morfologiche &egrave; molto diffusa. Per tratti semplici, come il colore generale del corpo, ripetute transizioni mediante mutazioni nello stesso gene possono essere comuni. Tuttavia, per tratti pi&ugrave; complessi, i possibili percorsi genetici possono essere pi&ugrave; numerosi; i meccanismi molecolari sottostanti le loro origini indipendenti e nella misura in cui essi sono vincolati a seguire determinati percorsi genetici sono in gran parte sconosciuti. Qui vi mostriamo che un pattern di pigmentazione ala maschile coinvolto nel rituale di corteggiamento &egrave; stato guadagnato e perso pi&ugrave; volte in un clade di Drosophila. Ognuno dei casi noi abbiamo analizzato (due guadagni e due perdite) coinvolti modifiche normative presso il gene pleiotropico pigmentazione gialla. Perdite coinvolto l&#39;inattivazione parallelo dello stesso elemento cis-regolatori (CRE), con le modifiche apportate a pochi nucleotidi sufficiente per spiegare la divergenza funzionale di un elemento tra due specie di pari livello. Sorprendentemente, due guadagni indipendenti di spot di ala &egrave; derivato dalla cooptazione dei distinti ancestrale di Cherso. Questi risultati dimostrano come la diversificazione funzionale di Cherso modulare di geni pleiotropici contribuisce alla novit&agrave; evolutiva e l&#39;evoluzione indipendente di somiglianze morfologiche.

Ripetuta evoluzione morfologica attraverso cambiamenti cis-regolatori in un gene pleiotropico.

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In many species, both morphological and molecular traits related to sex and reproduction evolve faster in males than in females. Ultimately, rapid male evolution relies on the acquisition of genetic variation associated with differential reproductive success. Many newly evolved genes are associated with novel functions that might enhance male fitness. However, functional evidence of the adaptive role of recently originated genes in males is still lacking. The Sperm dynein intermediate chain multigene family, which encodes a Sperm dynein intermediate chain presumably involved in sperm motility, originated from complex genetic rearrangements in the lineage that leads to Drosophila melanogaster within the last 5.4 million years since its split from Drosophila simulans. We deleted all the members of this multigene family resident on the X chromosome of D. melanogaster by chromosome engineering and found that, although the deletion does not result in a reduction of progeny number, it impairs the competence of the sperm in the presence of sperm from wild-type males. Therefore, the Sperm dynein intermediate chain multigene family contributes to the differential reproductive success among males and illustrates precisely how quickly a new gene function can be incorporated into the genetic network of a species.

Functional evidence that a recently evolved Drosophila sperm-specific gene boosts sperm competition.

In many animal species, traits associated with male fitness evolve rapidly. Intersexual conflict and male-male competition have been suggested to drive this rapid evolution. These fast evolutionary dynamics result in elevated rates of amino acid replacement and modification of gene expression attributes. Gene acquisition is another mechanism that might contribute to fitness differences among males. However, empirical evidence of fitness effects associated with newly evolved genes is scarce. The Sdic multigene family originated within the last 5.4 myr in the lineage that leads to D. melanogaster and encodes a sperm dynein intermediate chain presumably involved in sperm motility. The silencing of the Sdic multigene family, followed by the screening of relevant phenotypes, supports the role of the Sdic multigene family in sperm competition. The case of the Sdic multigene family illustrates the flexibility of genetic networks in incorporating lineage-specific gene novelties that can trigger an evolutionary arms race between males.

Shu-Dan Yeh

Department of Ecology and Evolutionary Biology

University of California, Irvine

Assessing Differences in Sperm Competitive Ability in Drosophila

Shu-Dan Yeh

.css-o250i3{font-size:18px;font-family:Open Sans,sans-serif;line-height:21.6px;}Department of Ecology and Evolutionary Biology

University of California, Irvine

Assessing Differences in Sperm Competitive Ability in Drosophila

Department of Ecology and Evolutionary Biology