Evolution without increased fitness

In our latest author blog, Dav­id N. Fish­er and Andrew G. McAdam explore how indir­ect genet­ic effects allow traits to evolve even in the absence of increased fit­ness across generations. 

Evol­u­tion by nat­ur­al selec­tion is the best way to under­stand how the amaz­ing and some­times bewil­der­ing diversity of life on earth came to be. Yet its core ideas are fairly simple. Those indi­vidu­als bear­ing the traits most suited to their envir­on­ment will sur­vive and repro­duce bet­ter (have high­er “fit­ness”), and so have more off­spring in the next gen­er­a­tion. If off­spring tend to resemble their par­ents then the next gen­er­a­tion will be com­prised of indi­vidu­als who bear the more bene­fi­cial traits, and there­fore the pop­u­la­tion as a whole will be bet­ter adap­ted to the envir­on­ment. We there­fore expect the aver­age fit­ness in the pop­u­la­tion in increase each gen­er­a­tion. We can sum­mar­ise this by say­ing we expect trait evol­u­tion to lead to adaptation.

How­ever, we can eas­ily observe situ­ations where it does not quite work like that. In a pop­u­la­tion of deer, males may com­pete for access to females. Increased antler size may allow deer to dom­in­ate oth­er males, giv­ing them increased access to females and so high­er repro­duct­ive suc­cess. The next gen­er­a­tion of males are there­fore more likely to be des­cend­ants of these more well-endowed males, and so will have lar­ger antlers them­selves. But do we expect aver­age fit­ness to increase? Not neces­sar­ily. In our example, while the aver­age male may have big­ger antlers, they are still com­pet­ing for access to the same num­ber of females (we’re assum­ing pop­u­la­tion size is not grow­ing here), who are repro­du­cing the same num­ber of off­spring. Aver­age male fit­ness is lim­ited by female repro­duc­tion, and so can­not increase. So, what has happened to our expect­a­tion that trait adapt­a­tion leads to evolution?

What has happened here, cryptic­ally, is that the social envir­on­ment has evolved. What we mean by this is that, while the aver­age male has lar­ger antlers, so too does any oth­er male he will com­pete with, as all are drawn from the same pop­u­la­tion. If a male in the new, big­ger-antlered, gen­er­a­tion was com­pet­ing with males from the old, smal­ler-antlered, gen­er­a­tion, he would be expec­ted to do bet­ter. But he isn’t, he is com­pet­ing against oth­er large antler males, also off­spring of suc­cess­ful males from the pre­vi­ous gen­er­a­tion. There­fore, any increase in antler size is coun­ter­ac­ted by increases in antler size of competitors.

While the evol­u­tion of the social envir­on­ment isn’t pre­dicted by stand­ard mod­els of evol­u­tion, it is by mod­els incor­por­at­ing “indir­ect genet­ic effects”. A dir­ect genet­ic effect is where the genes of an organ­ism influ­ences its own trait. An indir­ect genet­ic effect is where the genes of an organ­ism influ­ence the trait of anoth­er organ­ism. For example, when a mam­mali­an moth­er suckles her off­spring, her genes for milk pro­duc­tion will influ­ence how fast the off­spring grows. But indir­ect genet­ic effects apply much more broadly than that. Whenev­er organ­isms socially inter­act (e.g. court­ship and mat­ing, com­pet­ing for resources, influ­en­cing each other’s move­ment decisions, etc) we may expect indir­ect genet­ic effects to be present, and thus evol­u­tion to not con­form to stand­ard mod­els, as in our example with the deer above. When organ­isms inter­act, and the effect they have on each oth­er has a (at least partly) genet­ic basis, the lines between nature and nur­ture are blurred as the social envir­on­ment con­tains genes. There­fore, this social envir­on­ment can evolve.

While indir­ect genet­ic effects have been known for over 50 years, in our art­icle we apply them dir­ectly to fit­ness and assess the con­sequences. We find that by pre­dict­ing an increase in the com­pet­it­ive envir­on­ment across gen­er­a­tions, mod­els with indir­ect genet­ic effects on fit­ness can account for the lack of increase in mean fit­ness across gen­er­a­tions, even when oth­er traits are evolving. This obser­va­tion was not pre­vi­ously com­pat­ible with two fun­da­ment­al the­or­ems in evol­u­tion­ary bio­logy, R. A. Fisher’s fun­da­ment­al the­or­em of nat­ur­al selec­tion (which says that the rate of increase of mean fit­ness due to nat­ur­al selec­tion is equal to the genet­ic vari­ance in fit­ness), and G. R. Price’s cov­ari­ance equa­tion pre­dict­ing evol­u­tion change (when the evol­u­tion of a trait is equal to the genet­ic cov­ari­ance between the trait and fit­ness). This sug­gests indir­ect genet­ic effects on fit­ness could be fun­da­ment­al to under­stand­ing the evol­u­tion of pop­u­la­tions with any degree of com­pet­i­tion over a lim­ited resource. Social inter­ac­tions are every­where and there­fore indir­ect genet­ic effects on fit­ness may well be the norm rather than exceptions.

Fur­ther­more, indir­ect genet­ic effects could, in some extreme cir­cum­stances, cause fit­ness to evolve to be lower across gen­er­a­tions. This is known as “mal­ad­apt­a­tion” and is incom­pat­ible with Fisher’s fun­da­ment­al the­or­em of nat­ur­al selec­tion if indir­ect genet­ic effects are not con­sidered. Addi­tion­ally, in the math­em­at­ic­al equa­tions we use to under­stand how traits and fit­ness influ­enced by indir­ect genet­ic effects evolve, we mul­tiply the con­tri­bu­tion of the social envir­on­ment by the num­ber of inter­act­ing indi­vidu­als. So stronger effects on fit­ness from the social envir­on­ment are expec­ted when anim­als inter­act with more and more oth­er indi­vidu­als, i.e. as dens­it­ies increase. This then means indir­ect genet­ic effect mod­els for the evol­u­tion of fit­ness nat­ur­ally pre­dict dens­ity depend­ent repro­duc­tion! This remark­able con­nec­tion between genet­ic mod­els for social evol­u­tion and clas­sic mod­els for pop­u­la­tion growth help link sep­ar­ate but equally fun­da­ment­al areas of bio­logy, demon­strat­ing the util­ity of our approach. Finally, if there are indir­ect genet­ic effects on fit­ness, but not dir­ect genet­ic effects on fit­ness, then mean fit­ness may still be able to evolve, which was pre­vi­ously con­sidered impossible. This increases the range of situ­ations where we might expect adapt­a­tion to occur.

In sum­mary, con­sid­er­ing the evol­u­tion of the social envir­on­ment, and how there may be indir­ect genet­ic effects on fit­ness, recon­ciles two fun­da­ment­al ideas in evol­u­tion­ary bio­logy with obser­va­tions made in nature. Fur­ther­more, it serves to link mod­els for trait evol­u­tion to mod­els for pop­u­la­tion growth, and obser­va­tions of mal­ad­apt­a­tion or adapt­a­tion where it was pre­vi­ously thought to be impossible.

Dav­id N. Fish­er is a Postdoc­tor­al Research Asso­ci­ate and Andrew G. McAdam is an Asso­ci­ate Pro­fess­or, both in the Depart­ment of Integ­rat­ive Bio­logy at the Uni­ver­sity of Guelph. The ori­gin­al art­icle is freely avail­able to read and down­load from Evol­u­tion Letters