Genomic adaptation to life in extreme environments

Dr Dom­ino Joyce explains what her team’s new research tells us about how anim­als adapt to chal­len­ging envir­on­ments – and how quickly it can happen.

As we explore more of the earth’s extreme envir­on­ments, we learn more about how
organ­isms have adap­ted to life there. Many deep sea creatures have become famil­i­ar such as the vam­pire squid, spook­fish or blob­fish, and we are begin­ning to study their bio­lo­gic­al adapt­a­tions to dark, some­times cold, high pres­sure envir­on­ments. But there are also many less well stud­ied fresh­wa­ter envir­on­ments that pose sim­il­ar prob­lems for any organ­ism wish­ing to inhab­it them, and our work stud­ied a group of closely related deep water fish that live in Lake Malawi, in East Africa.

Lake_Malawi.jpg
Lake Malawi. Source: ESA, CC BY-SA 3.0 IGO, http://www.esa.int/spaceinimages/Images/2010/10/Lake_Malawi_Great_Rift_Valley

Lake Malawi is home to more than 800 dif­fer­ent spe­cies of cich­lid fishes, which is par­tic­u­larly impress­ive because they must have evolved in the lake some­time in the last 2–5 mil­lion years (they aren’t found any­where else, and before this time, the lake didn’t exist). These spe­cies are found in a range of envir­on­ments through­out the lake, from shal­low-water rocky reefs, where they have body, mouth and tooth shapes that help them scrape algae for nutri­tion, to the open water, where some spe­cies have become large and stream­lined pred­at­ors that chase and eat oth­er fish. We stud­ied four spe­cies of a deep water genus called Dip­lo­tax­odon, these fish are among the deep­est liv­ing cich­lids, found between 60 and 250 m, and they feed on zooplank­ton. We sequenced parts of their gen­ome, using a tech­nique called RAD-sequen­cing, to try to under­stand how their adapt­a­tions to depth have evolved.

Above: Cichlid fish from the deep water genus Diplotaxodon

Pos­it­ive selec­tion favours traits that increase an individual’s chances of sur­viv­al and/or
repro­duc­tion in a giv­en envir­on­ment. But envir­on­ments dif­fer and the traits that are adapt­ive in one envir­on­ment may be dif­fer­ent else­where. Genet­ic diver­gence between spe­cies nor­mally hap­pens very slowly over evol­u­tion­ary time, but may be accel­er­ated in gen­om­ic regions and genes that con­trol or are involved in the reg­u­la­tion of such adapt­ive traits. We com­pared DNA from a num­ber of indi­vidu­als from each of the four Dip­lo­tax­odon spe­cies, and found regions in the gen­ome that had diverged from one anoth­er very strongly com­pared to the aver­age gen­om­ic diver­gence, indic­at­ing that these regions may con­tain can­did­ate genes par­tic­u­larly import­ant for the evol­u­tion of these spe­cies and their sur­viv­al in their chal­len­ging environment.

Among these can­did­ates were genes involved in head and eye devel­op­ment. Some of our deep water spe­cies have rel­at­ively large eyes, which is thought to be adapt­ive in deep water envir­on­ments because lar­ger eyes increase the chances of cap­tur­ing the minute amounts of light that pen­et­rate the deep­er water lay­ers. We there­fore think this diver­gence may be a sig­na­ture that selec­tion has acted on these genes.

Anoth­er diver­gent region was centered around a gene which codes for a pro­tein in the lens of the eye – phakinin. We think that muta­tions in the sequence of this gene, which we were able to study thanks to the Sanger Centre, Cam­bridge, who shared some of their gen­om­ic data with us – affect the trans­par­ency of the eye lens, so that light can pass the lens more effi­ciently, thus rel­at­ively more light can reach the ret­ina and can be detec­ted by these fish in deep water.

Finally, we found a fur­ther diver­gent region that con­tained genes cod­ing for sub­units of the oxy­gen-car­ry­ing haemo­globin, and this lead us to exam­ine the par­tic­u­lar muta­tions in these genes too. We found con­sist­ent dif­fer­ences between vari­ants of these genes occur­ring in deep- and shal­low water spe­cies. Muta­tions in these genes have been shown in oth­er spe­cies, includ­ing humans, to affect the affin­ity of the haemo­globin molecules for bind­ing oxy­gen. Increased oxy­gen bind­ing affin­ity is anoth­er poten­tially adapt­ive trait in deep fresh­wa­ter envir­on­ments where the amount of dis­solved oxy­gen is rel­at­ively low. Most tele­ost fish pos­sess a so-called swim blad­der, a spe­cial­ized gas filled organ that allows them to con­trol their buoy­ancy in the water by act­ively reg­u­lat­ing the gas pres­sure in the blad­der. The great­er the water depth, the high­er the hydro­stat­ic pres­sure, the high­er the gas pres­sure in the blad­der needs to be to retain neut­ral buoy­ancy. Tele­osts have evolved a com­plex physiolo­gic­al sys­tem to ‘pump’ oxy­gen against a pres­sure gradi­ent from the blood into the blad­der. Cent­ral to the sys­tem is a phe­nomen­on known as the Root effect, which is the drastic reduc­tion of the oxy­gen car­ry­ing capa­city in response to slight changes in pH. In tele­osts spe­cial ‘Root haemo­globins’ trans­port and loc­ally release the oxy­gen used for inflat­ing the swim blad­der. The molecu­lar basis of the Root effect isn’t well under­stood yet, but we think that the muta­tions that we observe in the deep water spe­cies may facil­it­ate the pro­duc­tion of the high gas pres­sures that would be required in the deep.

Find­ing the parts of the gen­ome that have helped these fishes col­on­ise and adapt to the depths of Lake Malawi is inter­est­ing in itself, but it also demon­strates that at least some of the diversity in Lake Malawi cich­lids is a res­ult of “de novo” muta­tions that have aris­en in the lake and then been increased by selec­tion once proven advant­age­ous. That this can hap­pen in such a short evol­u­tion­ary time frame is impress­ive because we usu­ally asso­ci­ate such changes with a much longer timespan. But our work may also provide an insight into adapt­a­tions in oth­er liv­ing sys­tems- for example we would pre­dict that the lens clar­ity gene that has dif­fer­en­ti­ated in these spe­cies might have evolved in the same or sim­il­ar ways inde­pend­ently in large eyed deep water mar­ine fish. We might find import­ant muta­tions at the same points in the haemo­globin cod­ing genes of anim­als that have adap­ted in dif­fer­ent ways to oth­er chal­len­ging envir­on­ments, such as high altitude.

Identi­fy­ing the pos­sible muta­tion­al changes in the DNA that lead to adapt­a­tions to extreme envir­on­ments may help our under­stand­ing of par­tic­u­lar physiolo­gic­al pro­cesses, but also of evol­u­tion in gen­er­al. Find­ing these examples in Lake Malawi cich­lids means that we also now know that this type of adapt­a­tion can arise sur­pris­ingly quickly.

To learn more, read Dr Joyce’s paper, pub­lished open access in Evol­u­tion Letters.

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