Mating snails and population modelling: what can this tell us about the evolution of reproductive traits?

A new study pub­lished in Evol­u­tion Let­ters tests wheth­er rein­force­ment plays a role in the diver­gence of mat­ing pref­er­ence and gen­it­al mor­pho­logy dur­ing spe­ci­ation. Here, author Dr Maur­i­cio Montano-Ren­don explains what they found.

There is usu­ally more than one way to go about most things in life. Choos­ing a mate is cer­tainly one of them, with at least two options: ran­domly or non-ran­domly. In the second option, for instance, a pref­er­ence for a par­tic­u­lar size, shape, col­our, sound or smell may influ­ence the choice of mate. Addi­tion­ally, such a non-ran­dom way of mat­ing does not stay the same through­out time, but can change into new mat­ing pat­terns like, per­haps, when a wider vari­ety of mates becomes avail­able. Study­ing how non-ran­dom mat­ing evolves is cru­cial to our under­stand­ing of the pro­cesses whereby pop­u­la­tions evolve to become dis­tinct spe­cies, that is, the pro­cess of spe­ci­ation. The reas­on for this is that when there is a genet­ic pre­dis­pos­i­tion for choos­ing one type of mate over all oth­ers, and this pref­er­ence is passed on to the next gen­er­a­tions, then even­tu­ally that dif­fer­ence in pref­er­ence will form groups that no longer mate with each oth­er. As time goes by these groups could become dis­tinct species.

Apart from mat­ing pat­terns, there are oth­er repro­duct­ive char­ac­ter­ist­ics that can also have an impact in the pro­cess of spe­ci­ation. One of these is gen­it­al shape. Here the impact may be after mate choice, determ­in­ing wheth­er mat­ing will lead to suc­cess­ful fer­til­isa­tion. It has pre­vi­ously been observed that dif­fer­ences in such repro­duct­ive char­ac­ter­ist­ics, both mate choice and gen­it­al form, are com­monly more pro­nounced between closely related groups that coex­ist in the same region as opposed to those whose ranges do not over­lap. For example, choos­ing the right type of mate (that is the one you are genet­ic­ally pre­dis­posed to choose and that gives you more fit off­spring) is easi­er when you live sur­roun­ded only by the right type of mate; where­as if you live amongst two or more types of poten­tial mate then mak­ing the right choice is easi­er if the altern­at­ive types of mate dif­fer more strongly. The expec­ted pat­tern, great­er diver­gence in repro­duct­ive traits in areas of range over­lap, is known as repro­duct­ive char­ac­ter displacement.

Now, the really inter­est­ing bit is find­ing out how this pat­tern arises in the first place, and dis­crim­in­at­ing amongst the dif­fer­ent pos­sible causes is no simple task. In our new art­icle we address this fun­da­ment­al prob­lem using a mul­tidiscip­lin­ary approach. We think this provides an unusu­ally com­plete example where we aim to dis­tin­guish among three hypo­thes­ised pro­cesses that could lead to a pat­tern of repro­duct­ive char­ac­ter displacement.

Our study sys­tem was a pair of snail spe­cies, Lit­tor­ar­ia cin­gu­lata and L. filosa, nat­ive to the coastal man­grove forests of Aus­tralia. These are sis­ter spe­cies, each-oth­ers’ closest rel­at­ives. In the case of our snails, they are recently-formed and evolved sep­ar­ately, in geo­graph­ic isol­a­tion, and later on met each oth­er again as their ranges expan­ded after the last gla­ci­ation. The two spe­cies occur in sep­ar­ate geo­graph­ic­al areas, hav­ing only one region where they both cur­rently coex­ist. A pre­vi­ous study showed that they dif­fer more in gen­it­al form than oth­er sis­ter-spe­cies pairs in the same fam­ily that do not have over­lap­ping dis­tri­bu­tions. But, we did not know there was a great­er dif­fer­ence in gen­it­al form in this area of over­lap than where only one spe­cies is found, nor did we know how reli­ably the spe­cies could choose the right mate, either in the over­lap area or outside.

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Lit­tor­ar­ia filosa, one of the sis­ter snail spe­cies studied.

In the field, we con­duc­ted nearly one thou­sand one-to-one mat­ing tri­als sys­tem­at­ic­ally com­bin­ing snails from dif­fer­ent spe­cies and regions. We then recor­ded beha­viours such as the male mount­ing the female and penis inser­tion, and timed them. The longest cop­u­la­tion was 700 minutes (over 11.5 hours)! Sev­er­al vari­ables con­cern­ing the penis shape were also meas­ured. This was all a bit hard to explain to loc­al people we met on the Aus­trali­an coast!

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Field­work included sta­ging mat­ing tri­als and meas­ur­ing penis shape – and explain­ing all this to inter­ested passers-by!

We found a clear pat­tern of assort­at­ive mat­ing being strongest between pop­u­la­tions of the two spe­cies from the over­lap­ping geo­graph­ic­al area com­pared to all oth­er com­bin­a­tions. This is the expec­ted pat­tern of repro­duct­ive char­ac­ter dis­place­ment for mat­ing. How­ever, we could not demon­strate the same regard­ing penis shape: although the spe­cies dif­fer, they are no more dif­fer­ent over­all in the area of overlap.

Our three hypo­theses to explain repro­duct­ive char­ac­ter dis­place­ment were rein­force­ment, repro­duct­ive inter­fer­ence or the ‘Tem­pleton effect’. Rein­force­ment is the evol­u­tion of stronger assort­at­ive mat­ing or fer­til­isa­tion, and so stronger repro­duct­ive isol­a­tion, as a res­ult of selec­tion caused by the low fit­ness of hybrids. By con­trast, repro­duct­ive inter­fer­ence is a pro­cess of diver­gence between spe­cies caused by selec­tion to avoid wast­ing of repro­duct­ive effort on mat­ings that will gen­er­ate no off­spring. There­fore, the key dis­tinc­tion between these two pro­cesses comes from answer­ing the ques­tion: at the time when our two young spe­cies met each oth­er again, did they repro­duce with each oth­er and exchange genes?

The Tem­pleton effect sug­gests that pop­u­la­tions with­in each spe­cies diverged in mat­ing beha­viour or penis form before the two spe­cies came into con­tact. When con­tact hap­pens, it may be easi­er for the two spe­cies to coex­ist if they do not waste effort and gam­etes on inter­spe­cif­ic mat­ings. This can gen­er­ate a ‘fil­ter’ that only allows coex­ist­ence between more diver­gent pop­u­la­tions, pro­du­cing the same pat­tern of repro­duct­ive char­ac­ter dis­place­ment as the oth­er two processes.

To dis­tin­guish between rein­force­ment and repro­duct­ive inter­fer­ence, we turned to DNA sequen­cing and mod­el­ling of the his­tory of the pop­u­la­tions. Cut­ting a long story short, the genet­ic data were con­sist­ent with an his­tor­ic­al mod­el of geo­graph­ic sep­ar­a­tion dur­ing the ini­tial diver­gence of the two spe­cies and then some diver­gence between pop­u­la­tions with­in spe­cies, but not with any gene flow after renewed con­tact between the two spe­cies. This rules out rein­force­ment, which requires at least some gene exchange fol­low­ing con­tact. How­ever, we did find a first gen­er­a­tion hybrid between the two spe­cies. This is con­sist­ent with mat­ing inter­ac­tions and so with the selec­tion pres­sure needed to gen­er­ate repro­duct­ive char­ac­ter dis­place­ment by the pro­cess of repro­duct­ive interference.

The Tem­pleton effect is hard to exclude. Our mat­ing and penis shape res­ults sug­gest little diver­gence between pop­u­la­tions with­in spe­cies in either the sep­ar­ate or over­lap­ping parts of the range. The genet­ic data sug­gest con­tinu­ous gene flow between pop­u­la­tions with­in spe­cies. All of this argues against the diver­gence neces­sary to drive the Tem­pleton effect but can­not rule it out.

Many aspects of the pro­cess of spe­ci­ation remain con­tro­ver­sial. A role for rein­force­ment is now widely accep­ted but it is still very uncer­tain how often it con­trib­utes to the spe­ci­ation pro­cess or how import­ant it is in the evol­u­tion of repro­duct­ive isol­a­tion. While repro­duct­ive char­ac­ter dis­place­ment is a com­mon obser­va­tion, it is only when we can sep­ar­ate its pos­sible causes, as in our man­grove snails, that this obser­va­tion helps to determ­ine how spe­ci­ation occurs.

 

Dr Maur­i­cio Montano-Ren­don is an evol­u­tion­ary bio­lo­gist inter­ested in the pro­cesses shap­ing biod­iversity and lead­ing to the form­a­tion of new spe­cies. The ori­gin­al study is freely avail­able to read and down­load from Evol­u­tion Letters.