Phylogenetics of eggshell morphogenesis in Antheraea (lepidoptera: saturniidae): unique origin and repeated reduction of the aeropyle crown.
Integrated phylogenetic and developmental analyses should enhance our understanding of morphological evolution and thereby improve systematists' ability to utilize morphological characters, but case studies are few. The eggshell (chorion) of Lepidoptera (Insecta) has proven especially tractable experimentally for such analyses because its morphogenesis proceeds by extracellular assembly of proteins. This study focuses on a morphological novelty, the aeropyle crown, that arises at the end of choriogenesis in the wild silkmoth genus Antheraea. Aeropyle crowns are cylindrical projections, ending in prominent prongs, that surround the openings of breathing tubes (aeropyle channels) traversing the chorion. They occur over the entire egg surface in some species, are localized to a circumferential band in many others, and in some are missing entirely, thus exhibiting variation typical of discrete characters analyzed in morphological phylogenetics. Seeking an integrated developmental-phylogenetic view, we first survey aeropyle crown variation broadly across Antheraea and related genera. We then map these observations onto a robust phylogeny, based on three nuclear genes, to test the adequacy of character codings for aeropyle crown variation and to estimate the frequency and direction of change in those characters. Thirdly, we draw on previous studies of choriogenesis, supplemented by new data on gene expression, to hypothesize developmental-genetic bases for the inferred chorion character transformations. Aeropyle crowns are inferred to arise just once, in the ancestor of Antheraea, but to undergo four or more subsequent reductions without regain, a pattern consistent with Dollo's Law. Spatial distribution shows an analogous trend, though less clear-cut, toward reduction of coverage by aeropyle crowns. These trends suggest either that there is little or no natural selection on the details of the aeropyle crown structure or that evolution toward functional optima is ongoing, although no direct evidence exists for either. Genetic, biochemical, and microscopy studies point to at least two developmental changes underlying the origin of the aeropyle crown, namely, reinitiation of deposition of chorionic lamellae after the end of normal choriogenesis (i.e., heterochrony), and sharply increased production of underlying "filler" proteins that push the nascent final lamellae upward to form the crown (i.e., heteroposy). Identification of a unique putative cis-regulatory element shared by unrelated genes involved in aeropyle crown formation suggests a possible simple mechanism for repeated evolutionary reduction and spatial restriction of aeropyle crowns.
Regier
Jerome C
JC
Center for Biosystems Research, University of Maryland Biotechnology Institute, 5140 Plant Sciences Building, College Park, MD 20742, USA. regier@umd.edu
Paukstadt
Ulrich
U
Paukstadt
Laela H
LH
Mitter
Charles
C
Peigler
Richard S
RS
D000818:Animals; D001483:Base Sequence; D001499:Bayes Theorem; D015152:Blotting, Northern; D002262:Carboxy-Lyases / Q000235:genetics; D002823:Chorion / Q000502:physiology / Q000648:ultrastructure*; D017931:DNA Primers; D018507:Gene Expression Regulation, Developmental; D046529:Microscopy, Electron, Transmission; D008957:Models, Genetic; D008969:Molecular Sequence Data; D009024:Morphogenesis; D009036:Moths / Q000033:anatomy & histology* / Q000235:genetics / Q000502:physiology*; D009687:Nuclear Proteins / Q000235:genetics; D010063:Ovum / Q000166:cytology*; D020648:Peptide Elongation Factor 1 / Q000235:genetics; D056950:Period Circadian Proteins; D010802:Phylogeny; D017422:Sequence Analysis, DNA; D013045:Species Specificity
D017931:DNA Primers; D009687:Nuclear Proteins; D020648:Peptide Elongation Factor 1; D056950:Period Circadian Proteins; D002262:Carboxy-Lyases; C477392:L-3,4-dihydroxyphenylalanine decarboxylase, Bombyx mori