Different different but same: Parallel evolution of gene expression in Caribbean Pupfishes

Guest author post: Joe McGirr tells Evolution Letters how two very different Cyprinodon pupfish species have a surprising amount in common.

The phrase “Same same but dif­fer­ent” is some­thing you might hear while back­pack­ing across south­east Asia. For example, a couple of sum­mers ago I found myself in a small shop in Bangkok hag­gling for a cheap watch. Here’s part of the con­ver­sa­tion I had with the shop owner:

Me: “Are these genu­ine Rolex watches you have for sale?”

Own­er: “Oh yes. Same same but different.”

The own­er meant that his watches were nearly indis­tin­guish­able from a real Rolex, but they were still dif­fer­ent in import­ant ways.

In nature, we often find spe­cies that are “same same but dif­fer­ent” when two diver­gent lin­eages evolve par­al­lel traits adap­ted to sim­il­ar envir­on­ments. For example, two darkly colored spe­cies might evolve light­er pig­ment­a­tion as an adapt­a­tion to a white sand envir­on­ment (see Rosen­blum and Har­mon 2010). How­ever, it’s not always obvi­ous that two spe­cies have evolved par­al­lel adap­tions just by look­ing at them. Some­times it would be more appro­pri­ate to describe spe­cies as “dif­fer­ent dif­fer­ent but same.”

I’ll explain.

In our new paper pub­lished in Evol­u­tion Let­ters, we study two recently diverged Cyp­rinodon pup­fish spe­cies endem­ic to San Sal­vador Island, Bahamas. At first glance, you might not expect to find much in com­mon between C. desquam­at­or – a ‘scale-eat­er’ spe­cies that has evolved large oral jaws spe­cial­ized for tear­ing scales off of oth­er pup­fishes, and C. bron­totheroides – a ‘snail-eat­er’ spe­cies that evolved robust short jaws and a max­il­lary pro­tru­sion for crush­ing mol­lusks. Cyp­rinodon pup­fishes are found through­out the Carib­bean, but they are largely diet­ary gen­er­al­ists that con­sume mac­roal­gae and detrit­us. Scale-eat­ing and snail-eat­ing niches are entirely unique to these spe­cial­ists on San Sal­vador, and they likely diverged from a gen­er­al­ist com­mon ancest­or with­in the last 10,000 years.

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Cyp­rin­don pup­fish: gen­er­al­ist C. varie­gat­us (top), snail-eat­er C. bron­totheroides (middle), and scale-eat­er C. desquam­at­or (bot­tom). Pho­tos by Emilie Richards.

Giv­en that scale-eat­ers and snail-eat­ers diverged so recently and yet dif­fer so dra­mat­ic­ally in their diet and cra­ni­al mor­pho­logy, we wanted to know how sim­il­ar these spe­cies were at a genet­ic level. We com­pared gene expres­sion of each spe­cies with a closely related gen­er­al­ist sis­ter spe­cies that is found along­side spe­cial­ists on San Sal­vador Island.

We were sur­prised to find that the scale-eat­er and snail-eat­er spe­cies showed remark­ably sim­il­ar gene expres­sion pat­terns rel­at­ive to the gen­er­al­ist spe­cies. Spe­cific­ally, 80% of genes that showed expres­sion dif­fer­ences between the snail-eat­er and gen­er­al­ist spe­cies showed the same expres­sion dif­fer­ences between the scale-eat­er and gen­er­al­ist spe­cies. This is excit­ing because it is the first example of a strange pat­tern: we find par­al­lel changes in gene expres­sion under­ly­ing diver­gent diet­ary specialization.

This is why I like to call scale-eat­ers and snail-eat­ers spe­cies “dif­fer­ent dif­fer­ent but same”. They spe­cial­ize on dif­fer­ent resources, show diver­gent cra­ni­al mor­pho­logy, but look very sim­il­ar to each oth­er at the level of gene expression.

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Micro-CT scans show­ing drastic craniofa­cial mor­pho­lo­gic­al diver­gence between snail-eat­ers (top) and scale-eat­ers (bot­tom). Images mod­i­fied from Hernan­dez et al. 2017 DOI: 10.1111/joa.12742

To try to under­stand why these spe­cial­ist spe­cies show par­al­lel changes in gene expres­sion, we thought about how scale-eat­ers and snail-eat­ers are more sim­il­ar to each oth­er than either is to their gen­er­al­ist sis­ter spe­cies. For example, the spe­cial­ists occupy a high­er troph­ic level than gen­er­al­ist spe­cies, mean­ing that spe­cial­ist diets con­tain less algae and more anim­al derived nutri­ents. We found that many genes show­ing par­al­lel changes in expres­sion were known to affect nitro­gen meta­bol­ism in oth­er mod­el organ­isms. This makes sense because scales and snails both con­trib­ute to diets that are high­er in nitro­gen com­pared to a gen­er­al­ist diet, sug­gest­ing that spe­cial­ist spe­cies show par­al­lel evol­u­tion of gene expres­sion as a par­al­lel adap­tion to a high­er troph­ic level.

These find­ings add to our know­ledge of the types of par­al­lel adapt­a­tions that arise dur­ing spe­ci­ation, and high­light how spe­cies can evolve sim­il­ar gene expres­sion des­pite diver­gent diet­ary specialization.

 

Joe McGirr is a gradu­ate stu­dent at the Depart­ment of Bio­logy, Uni­ver­sity of North Car­o­lina at Chapel Hill. His study is freely avail­able to read and down­load from Evol­u­tion Let­ters.

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