Academic journal article Genetics

Genetic Basis of a Violation of Dollo's Law: Re-Evolution of Rotating Sex Combs in Drosophila Bipectinata

Academic journal article Genetics

Genetic Basis of a Violation of Dollo's Law: Re-Evolution of Rotating Sex Combs in Drosophila Bipectinata

Article excerpt

ABSTRACT Phylogenetic analyses suggest that violations of "Dollo's law"-that is, re-evolution of lost complex structures-do occur, albeit infrequently. However, the genetic basis of such reversals has not been examined. Here, we address this question using the Drosophila sex comb, a recently evolved, male-specific morphological structure composed of modified bristles. In some species, sex comb development involves only the modification of individual bristles, while other species have more complex "rotated" sex combs that are shaped by coordinated migration of epithelial tissues. Rotated sex combs were lost in the ananassae species subgroup and subsequently re-evolved, ~12 million years later, in Drosophila bipectinata and its sibling species. We examine the genetic basis of the differences in sex comb morphology between D. bipectinata and D. malerkotliana, a closely related species with a much simpler sex comb representing the ancestral condition. QTL mapping reveals that >50% of this difference is controlled by one chromosomal inversion that covers ~5% of the genome. Several other, larger inversions do not contribute appreciably to the phenotype. This genetic architecture suggests that rotating sex combs may have re-evolved through changes in relatively few genes. We discuss potential developmental mechanisms that may allow lost complex structures to be regained.

DOLLO'S "law of irreversibility" posits that complex morphological structures, once lost during evolution, cannot be regained in the same form. This principle makes intuitive sense: resurrecting an extinct developmental pathway in close to its ancestral condition seems biologically as well as statistically implausible. And yet, phylogenetic analyses have revealed several cases where Dollo's law is apparently violated. Examples include re-evolution of lost digits in lizards (Kohlsdorf and Wagner 2006; Brandley et al. 2008; Kohlsdorf et al. 2010), eggshells and oviparity in boas (Lynch and Wagner 2010), wings in stick insects (Whiting et al. 2003), shell coiling in limpets (Collin and Cipriani 2003), mandibular teeth in frogs (Wiens 2011), molars in lynx (Kurten 1963), and others. There is a growing consensus that lost structures can sometimes be regained, especially if that happens soon after the initial loss (Wiens 2011) (but see Goldberg and Igic 2008 and Galis et al. 2010 for counterarguments). This shifts the question from the realm of phylogenies to developmental genetics: how can complex structures re-evolve? What is the genetic basis of such reversals?

In this report, we examine the genetic basis of a likely violation of Dollo's law that occurred during the evolution of Drosophila sex combs. Sex combs are male-specific arrays of modified mechanosensory bristles ("teeth") that evolved within the genus Drosophila and are used by males during courtship and mating (Kopp 2011). These structures develop from either transverse or longitudinal bristle rows that are present on the front legs of both sexes and show extensive morphological diversity but essentially fall into three distinct types. "Rotating" sex combs develop from one or several transverse bristle rows (TBRs) that undergo a 90~ rotation. This rotation is driven by a precisely coordinated rearrangement of several hundred epithelial cells that, assisted by strong homophilic adhesion between adjacent bristle cells, moves the embedded bristle rows from a transverse to a more longitudinal orientation (Atallah et al. 2009a,b; Tanaka et al. 2009). In contrast, "transverse" sex combs are simply TBRs composed of modified bristles. In this case, sex comb development is limited to the modification of individual bristle shafts and does not involve any morphogenetic movements (Kopp 2011). Finally, "longitudinal" sex combs resemble rotating sex combs in adult flies but actually develop from longitudinal bristle rows and are not homologous to the rotating sex combs on a cell-by-cell basis (Atallah et al. …

Search by... Author
Show... All Results Primary Sources Peer-reviewed

Oops!

An unknown error has occurred. Please click the button below to reload the page. If the problem persists, please try again in a little while.