Twisted sex overcomes barriers to gene flow in mirror image snails

A new study in Evol­u­tion Let­ters has shown that two types of snails are the same spe­cies, des­pite pre­vi­ously being con­sidered dis­tinct because their shells coil in the oppos­ite dir­ec­tion. Not only are the snails genet­ic­ally sim­il­ar, but sur­pris­ingly, they are able to have sex des­pite their phys­ic­al dif­fer­ences. Here Dr Angus Dav­is­on, one of the study’s authors, tells us more about twis­ted snail sex and its evol­u­tion­ary implications.

EL: One of the key find­ings of your study was that some mir­ror-image snails, which coil in dif­fer­ent dir­ec­tions due to the effects of a single gene, can have sex des­pite being rather mis­aligned. How does that work?

AD: Most land snails with low spired snails – includ­ing garden snails and Cepaea – mate in a face-to-face pos­i­tion, and are sim­ul­tan­eous herm­aph­rod­ites, so mate as male and female at the same time. In nor­mal right-coil­ing snails (dex­trals), the gen­it­als are on the right hand side of the head, so that when two snails mate, the two right sides come togeth­er, and their gen­it­als are inser­ted reciprocally.

If a com­mon dex­tral snail meets a rare sin­is­tral ‘lefty’ snail, the snails try to mate as nor­mal – but the parts don’t fit togeth­er as expec­ted. You could liken it to try­ing to shake a left hand, everything is in the wrong pos­i­tion and it is very awk­ward. A fur­ther ana­logy might be to think of that scene in films where car-driv­ing drug deal­ers meet in a park­ing lot to exchange pack­ages, by wind­ing down their win­dows and reach­ing across. This only works if they are both in right-hand or left-hand drive cars. The same may be true for snails, except of course they are trad­ing sper­ma­to­phores, rather than drugs.

EL: Why do they have to mate face-to-face?

AD: That is a great ques­tion! I think that the key point is that in face-to-face mat­ing, cop­u­la­tion only takes place if actions are recip­roc­ated, mean­ing that both mat­ing part­ners are obliged to act as male and female at the same time. I think that for these snails – as in humans – main­tain­ing mutu­al com­mu­nic­a­tion prob­ably works best in a face-face position

Some oth­er snails mate in a dif­fer­ent pos­i­tion: one snail mounts the oth­er from behind and takes a male role, with the oth­er being female. After a first mat­ing, they may reverse the pro­cess and switch sex roles – but there is no obligation.

EL: We often claim that oppos­ites attract, but these tricky sexu­al encoun­ters sound off-put­ting. Do these snails gen­er­ally prefer to have sex with sim­il­arly coiled mates?

AD: The lim­ited evid­ence that we have sug­gests that while a snail has know­ledge of its own chir­al­ity, because of the chir­al move­ments that they make dur­ing court­ship, I don’t think that they can sense the coil­ing dir­ec­tion of anoth­er snail. This is prob­ably what leads to the fum­bling that we see when lefties and righties try to mate – they will try repeatedly, but without suc­cess. Unfor­tu­nately, we have almost no data on mat­ing fre­quen­cies, partly because encoun­ters between lefties and righties are so rare.

In snails such as the garden snail, and Japan­ese Euhadra, it has been com­monly assumed that dex­tral and sin­is­tral are not able to mate, argu­ably mak­ing them sep­ar­ate spe­cies. One con­sequence of not being able to mate is that the rarer type of snail will tend not to have off­spring and so the under­ly­ing chir­al­ity-determ­in­ing allele will not be passed on. This fre­quency-depend­ent selec­tion partly explains why most snails only coil one way, and why closely related but dif­fer­ently coil­ing Euhadra do not occur togeth­er, except in nar­row con­tact zones, across Japan. How­ever, the oth­er inter­est­ing part of the explan­a­tion for the dom­in­ance of one type of snail is that muta­tions at the chir­al­ity gene locus can affect sev­er­al dif­fer­ent traits at once (pleio­tropy). This means that it is simply very dif­fi­cult to change chir­al­ity without mak­ing dele­ter­i­ous changes to oth­er char­ac­ter­ist­ics of the snails, espe­cially dur­ing early development.

Finally, we might sup­pose that the reas­on sin­is­trals and dex­trals are not able to mate is because the gen­it­als don’t fit togeth­er in a phys­ic­al sense. How­ever, Menno Schilthuizen has shown in Amphidro­mus snails that it is more a beha­vi­our­al issue. As the gen­it­als are long, thin, flex­ible organs, it is not a prob­lem for them to twist into pos­i­tion – it is just that the snail does not know how to do this, because it is not aware of the prob­lem in the first place.

EL: Your work chal­lenges the pre­vi­ous con­sensus that cer­tain mir­ror-image snails con­sti­tute dif­fer­ent spe­cies. Anim­als are gen­er­ally con­sidered to be the same spe­cies if they can pro­duce viable off­spring, not just if they can phys­ic­ally cop­u­late. Do your mir­ror-image snails repro­duce successfully?

AD: We have no dir­ect evid­ence that the left and right coil­ing Euhadra that we stud­ied are able to pro­duce viable off­spring when they do occa­sion­ally mate. How­ever, the evid­ence is in the DNA – we used a tech­nique called Restric­tion site Asso­ci­ated DNA sequen­cing (RAD-seq) to sur­vey their gen­omes, which con­firmed that there is move­ment of genes between the two types.

As a genet­i­cist, the inter­est­ing aspect of this study is that the expres­sion of the snail chir­al­ity gene is delayed by a gen­er­a­tion, due to ‘mater­nal inher­it­ance’, fam­ously first described in the 1920s. In a sim­il­ar way that the shell col­our of a bird’s egg is determ­ined by the moth­er, rather than the off­spring inside the egg, the early embryon­ic switch to dex­tral or sin­is­tral, and the later coil­ing dir­ec­tion of a snail, is determ­ined only by the moth­er. One curi­ous con­sequence of this mater­nal inher­it­ance is that it can lead to dis­con­nect between phen­o­type and under­ly­ing gen­o­type, so a snail with a dex­tral coil­ing shell might be genet­ic­ally homo­zyg­ous sin­is­tral, and thus bear sin­is­tral off­spring. This dis­cord is a fur­ther indir­ect route by which the two types exchange genes.

Our final con­clu­sion, which I hope oth­ers agree with, is that changes in chir­al­ity are insuf­fi­cient on their own to cause spe­ci­ation – oth­er factors are required.

EL: Does the dir­ec­tion in which a snail coils impact any oth­er aspect of its life, oth­er than who it can mate with?

AD: Pre­vi­ously, we found a muta­tion in pond snails which determ­ines wheth­er they coil to the left or right, but in that spe­cies the mutant sin­is­trals have a poor hatch rate com­pared with dex­trals, mak­ing it unlikely that they will ever reach a high fre­quency – so this muta­tion is not import­ant in an evol­u­tion­ary sense. For me, the most fas­cin­at­ing thing would be to find the genes that determ­ine the dif­fer­ences in chir­al­ity in spe­cies such as Euhadra, per­haps via a gen­ome wide asso­ci­ation study (GWAS) which would allow us to find genet­ic vari­ants that are asso­ci­ated with this par­tic­u­lar trait. The interest is pre­cisely because the chir­al switch has no oth­er impact upon these snails’ lives.

EL: Are there any oth­er anim­als in which body plan asym­metry can be reversed? What are the consequences?

AD: The amaz­ing thing is that no oth­er anim­als com­monly vary in their asym­metry, except per­haps a few nem­at­odes. Why? I think that it again comes down to pleio­tropy (when a gene influ­ences mul­tiple seem­ingly unre­lated traits) – it is simply very dif­fi­cult to reverse asym­metry without mak­ing oth­er dele­ter­i­ous changes. At this moment, it is not clear why snails are able to vary their chir­al­ity, nor which genes are involved in mak­ing these changes – but I would love to find out.

Ulti­mately, these stud­ies may have some con­sequence in under­stand­ing human devel­op­ment – although only about one in ten thou­sand per­sons is a mir­ror-image intern­ally (includ­ing Enrique Iglesi­as and Donny Osmond), organ pos­i­tion­ing defects are a rel­at­ively com­mon cause of pre-term loss of embry­os. Although study­ing snails is not going to cure any prob­lems caused by pos­i­tion­ing defects, longer term research will con­trib­ute to an under­stand­ing of the estab­lish­ment of left-right asym­metry, espe­cially in find­ing com­mon­al­it­ies in the devel­op­ment of these diverse organisms.

If these snails are a single spe­cies, how did the two mir­ror-image types arise in the first place? Which one came first?

A chick­en and egg ques­tion – but one which we can prob­ably answer! Although snails have switched chir­al­ity mul­tiple times, the vast major­ity of snail spe­cies are still right-coil­ing (or dex­tral). My guess is that the very first snail to become estab­lished was right coil­ing, and it is simply dif­fi­cult to change.

There are some clues as to why it might some­times be an advant­age to change chir­al­ity, des­pite the dif­fi­culties. One explan­a­tion is that being sin­is­tral means that a snail does not have unpro­duct­ive mat­ings with closely related spe­cies liv­ing in the same geo­graph­ic­al area – such may be the case in Euhadra. Anoth­er intriguing explan­a­tion, provided by a col­league Masaki Hoso, is that being sin­is­tral reduces the chance of being pred­ated by a snake, which fits with the obser­va­tion that there is a rel­at­ively high pro­por­tion of sin­is­tral snails in East Asia where the snake is found.

Dr Angus Dav­is­on is Asso­ci­ate Pro­fess­or and Read­er in Evol­u­tion­ary Genet­ics at the School of Life Sci­ences, Uni­ver­sity of Not­ting­ham. The study is freely avail­able to read and down­load via Evol­u­tion Let­ters Early View.