Genetic Basis of a Violation of Dollo’s Law: Re-Evolution of Rotating Sex Combs inDrosophila bipectinata

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 andIgic 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 essenti...

Repeated horizontal gene transfer ofGALactose metabolism genes violates Dollo’s law of irreversible loss

“…For more than a century, trait reversal after a loss event has been thought to be highly unlikely; Dollo's law of irreversibility states that, once a trait is lost, it is unlikely for the same trait to be found in a descendant lineage, thereby excluding certain evolutionary paths 5,6 . Despite this purist interpretation, many examples of apparent violations to Dollo's law have been documented [7][8][9][10][11][12][13][14][15] , and it is clear that evolutionary processes sometimes break Dollo's law [16][17][18] . Nonetheless, the molecular and genetic mechanisms leading to trait reversal have only been determined in a few cases 17,18 .…”

Trpc2 pseudogenization dynamics in bats reveal ancestral vomeronasal signaling, then pervasive loss

“…Dollo describes evolution as "irreversible" and "discontinuous," and trait complexity prevents evolution from returning organisms to their previous state. Few studies have actually turned to the molecular mechanisms determining trait function (Sassi et al 2007;Christin and Besnard 2009;Seher et al 2012), or the selective forces shaping traits. These studies infer the re-evolution of traits after ancestral loss, sometimes multiple times.…”

“…Those analyses remain controversial, however, as unsuitable inference methods have been used, and the true complexity of traits is often ignored (Goldberg and Igić 2008). Few studies have actually turned to the molecular mechanisms determining trait function (Sassi et al 2007;Christin and Besnard 2009;Seher et al 2012), or the selective forces shaping traits. Here, we analyze the molecular evolution of a mammalian chemosensory system, examining changes in selection underlying the loss of this complex system throughout the diversification of bats.…”

Contrasting models of parity‐mode evolution in squamate reptiles

“…Conversely, it may be found that the promoter regions or other regulatory complexes responsible for eggshells are simply switched off during the transition to viviparity, but are maintained by selection in a functional or dormant state in the genome of viviparous lineages, and need only be reactivated or re‐formulated for the eggshell to be regained. Such a process (re‐activation of functional gene‐complexes) has been commonly reported as a mechanism for the regain of complex traits in other organisms, such as sex combs in Drosophila (Seher et al, ), hand musculature in primates (Diogo and Wood, ), and sexuality in oribatid mites (Domes et al, ).…”