Two thirds of morphological changes in Drosophila are evolutionarily repetitive

A new study pub­lished in Evol­u­tion Let­ters has shed light on the lim­its of mor­pho­lo­gic­al evol­u­tion. Here, author Amir Yassin tells us more.

Nearly 150 years ago, Charles Dar­win exal­ted about the ‘end­less forms’ of life that evol­u­tion has pro­duced. How­ever, recent stud­ies have indic­ated that sev­er­al bio­lo­gic­al forms repeatedly evolved in dis­tant lin­eages, such as wings in birds and bats, reduced leaves in desert plants, or fusi­form body shapes in fishes and sea-dwell­ing mam­mals. Some authors have claimed that this phe­nomen­on, known as homo­plasy, was so fre­quent that mor­pho­lo­gic­al evol­u­tion may indeed be lim­ited and a sort of a pre­dict­able ‘peri­od­ic table’ of forms could be recon­struc­ted for all liv­ing organisms.

Through­out the his­tory of life, both phe­nom­ena of homo­plasy and innov­a­tion occurred, but an apprais­al of their fre­quen­cies at the mor­pho­lo­gic­al level remains lack­ing. Indeed, long lists of homo­plastic char­ac­ters across wide range of spe­cies have been com­piled but equi­val­ent lists for all mor­pho­lo­gic­al changes have yet to be made. The lack of such lists partly arises from the com­plex­ity by which mor­pho­lo­gic­al char­ac­ters could be con­ceived and vari­ab­il­ity with­in which could be cat­egor­ized into well-defined states. Indeed, mor­pho­lo­gic­al descrip­tions of most spe­cies are usu­ally scattered in the taxo­nom­ic lit­er­at­ure with few attempts to cur­ate these descrip­tions into com­par­at­ive tables or databases.

We there­fore decided to study mor­pho­lo­gic­al evol­u­tion in 56 fly spe­cies belong­ing to the fam­ily Dro­so­phil­id­ae, which encom­passes Dro­so­phila melano­gaster, one of the most stud­ied insects in devel­op­ment­al bio­logy and genet­ics. We con­cep­tu­al­ized 490 mor­pho­lo­gic­al char­ac­ters from descrip­tions in two excel­lent taxo­nom­ic books includ­ing both pre-adult stages (such as eggs, lar­vae and pupae) and adults. We also designed stat­ist­ic­al meth­ods to code vari­ation with­in each of these char­ac­ters into numer­ic­al classes or states. We then inferred a molecu­lar phylo­gen­et­ic tree of these spe­cies based on five genes, and coun­ted the num­ber of changes, from one state to anoth­er, in each mor­pho­lo­gic­al char­ac­ter upon the molecu­lar tree.

drosophilidae4

We found that two thirds of the mor­pho­lo­gic­al changes led to the repet­it­ive ori­gin of the same char­ac­ter state in dis­tant spe­cies, where­as one third of the changes begot a unique nov­el states. These changes were not ran­domly dis­trib­uted among the char­ac­ters. For example, homo­plastic or repet­it­ive changes were high­er in pre-adult stages than in adults. On the oth­er hand, unique nov­el traits were more fre­quent in male and female gen­italia than in oth­er adult body parts (such as eyes, legs or wings), most likely due to the strong sexu­al selec­tion act­ing on repro­duct­ive organs. We also revealed a strong stas­is in mor­pho­lo­gic­al evol­u­tion. When any pair of spe­cies was ran­domly chosen, only 13% of their sim­il­ar char­ac­ter states were homo­plastic, indic­at­ing that the great major­ity of their mor­pho­lo­gic­al sim­il­ar­it­ies were inher­ited from a last com­mon ancest­or rather than being due to inde­pend­ent origins.

Although our study pro­duced one of the longest mor­pho­lo­gic­al char­ac­ter lists in an anim­al fam­ily, we hypo­thes­ized from devel­op­ment­al bio­lo­gic­al stud­ies in Dro­so­phila melano­gaster alone that the total num­ber of mor­pho­lo­gic­al char­ac­ters that could be stud­ied in mul­tiple spe­cies far exceeds our list of 490 char­ac­ters. Non­ethe­less, our study rep­res­ents a first step towards cur­at­ing this diversity. Giv­en the unique genet­ic tools avail­able for this labor­at­ory mod­el, the recon­struc­tion of mor­pho­lo­gic­al data­bases would defin­it­ively pro­mote and facil­it­ate the iden­ti­fic­a­tion of the molecu­lar under­pin­nings and devel­op­ment­al path­ways under­ly­ing the evol­u­tion of both repet­it­ive and nov­el mor­pho­lo­gic­al states in Dro­so­phila and pos­sibly beyond.

Amir Yassin is a CNRS Research Officer at the Nation­al Museum of Nat­ur­al His­tory, Par­is. The ori­gin­al art­icle is freely avail­able to read and down­load here.