Fishes famed for being bony have soft spot

Eli G. Cytryn­baum, Clayton M. Small, and Charles B. Kim­mel, authors of a new study in Evol­u­tion Let­ters, explain how their dis­cov­ery of the “exten­ded osteoid” – a non­min­er­al­ised bone mat­rix – influ­ences our under­stand­ing of mor­pho­lo­gic­al evol­u­tion in bony fish.

Scul­pins are benthic fish in the super­fam­ily Cot­toidea famed for their boni­ness. Often a bane of sport fish­ers, scul­pins sit on the bot­toms of streams, lakes, tide­pools and even the open ocean and steal bait – only to be too much of a bot­tom dwell­er to offer a good fight and mostly too spiny to make a good meal. With great cam­ou­flage and large spines, they deter many a pro­spect­ive pred­at­or and have, with­in a rel­at­ively recent evol­u­tion­ary time frame, under­gone a massive radi­ation as they have adap­ted to the range of hab­it­ats they now occupy. This rel­at­ively rap­id diver­si­fic­a­tion in both mor­pho­logy and life his­tory makes sculpin a great mod­el in which to explore the dynam­ics of evol­u­tion, sim­il­ar to the famed cich­lids of east­ern Africa. We have dis­covered that one mech­an­ism by which these fishes full of prickles and hard bits have been able to achieve such rap­id shifts in mor­pho­logy may be related to a dis­tinctly soft modi­fic­a­tion: scul­pins and a few of their rel­at­ives exhib­it tar­geted lack of min­er­al­iz­a­tion in cer­tain bone tis­sues, allow­ing for fine tun­ing of bone mor­pho­logy without chan­ging the recruit­ment or place­ment of bone cells dur­ing development.

Bones serve as the scaf­fold­ing upon which the rest of the body takes form. As a res­ult, bone shape and size con­sti­tute fun­da­ment­al com­pon­ents of over­all mor­pho­lo­gic­al diversity in these organ­isms. Many of the mech­an­isms which pro­duce vari­ation in bone shape on an evol­u­tion­ary scale are based on dif­fer­ences in the place­ment of osteo­blasts, bone pro­gen­it­or cells respons­ible for the form­a­tion and min­er­al­iz­a­tion of bone mat­rix to pro­duce rigid bone. Changes in the spa­ti­otem­por­al place­ment of osteo­blasts can be accom­plished via con­trolling the pro­lif­er­a­tion of osteo­blasts, their migra­tion from place to place, or even by con­vert­ing oth­er cell types to pro­duce bone mat­rix and has been observed in mod­els ran­ging from zebrafish to mice and beyond.

Along with alter­ing pre­lim­in­ary bone mat­rix mor­pho­logy, we found that scul­pins and some related fish employ a com­pletely dif­fer­ent strategy to modi­fy bone shape. They pro­duce sig­ni­fic­ant mor­pho­lo­gic­al vari­ation by leav­ing spe­cif­ic swaths of bone mat­rix non­min­er­al­ized, to turn what would have been rigid bone into a floppy membrane.

Bone mat­rix first devel­ops as a flex­ible, non­min­er­al­ized mem­brane – referred to as osteoid. The mem­brane – rarely more than a few cells thick – is present on the grow­ing sur­face of a bone and pro­duced by osteo­blasts that are recruited or pro­lif­er­at­ing. In most spe­cies, and in most sculpin bones, osteoid lasts for a van­ish­ingly brief peri­od of time before min­er­al­iz­ing and thus becom­ing the rigid mater­i­al we asso­ci­ate with bone tis­sue. Cer­tain dis­orders reduce the extent to which bones min­er­al­ize, and some muta­tions or the lack of key nutri­ents have even been found to stop min­er­al­iz­a­tion through­out the body. How­ever, in many spe­cies of scul­pins, a region on the bones of their gill cov­er, in par­tic­u­lar a bone known as the opercle, the osteoid remains non­min­er­al­ized as it grows. By fine tun­ing min­er­al­iz­a­tion and bone devel­op­ment care­fully enough to leave a vari­able patch of bone mat­rix non­min­er­al­ized with­in a lar­ger bone where the rest of the tis­sue is nor­mally min­er­al­ized, scul­pins have been able to achieve drastic­ally var­ied bone mor­pho­logy, seem­ingly without alter­ing the spa­ti­otem­por­al dis­tri­bu­tion of osteoblasts.

This non­min­er­al­ized bone mat­rix – which we dubbed “exten­ded osteoid” for the man­ner in which it extends the bone devel­op­ment­al stage of osteoid both spa­tially and tem­por­ally – appears to dif­fer­ent extents in vari­ous sculpin lin­eages. In cer­tain spe­cies the entire main oper­cu­lar bone is min­er­al­ized, giv­ing it a fan shape, while in oth­er spe­cies exten­ded osteoid com­poses the entire middle por­tion, mak­ing the bone a rigid fork with a flex­ible sail in between. We observed the fork phen­o­type in all sur­veyed fresh­wa­ter and inter­tid­al scul­pins along with some sub­tid­al mar­ine spe­cies, and the exten­ded osteoid tis­sue respons­ible for this “fork­i­ness” is a major con­trib­ut­or to the mor­pho­lo­gic­al vari­ation of the bone.

Oper­cu­lar exten­ded osteoid gives us a won­der­ful mod­el for study­ing evol­u­tion­ary dynam­ics, espe­cially as it appears to have aris­en sev­er­al times inde­pend­ently across the phylo­geny. Moreover, it provides an oppor­tun­ity to explore the mech­an­isms under­ly­ing bone devel­op­ment and min­er­al­iz­a­tion as typ­ic­al osteoid is so small and transient.

Many ques­tions still remain, such as what select­ive agents may have led to the repeated evol­u­tion of this phen­o­type and what path­ways are involved in the main­ten­ance of exten­ded osteoid dur­ing devel­op­ment. This nov­el mater­i­al holds great poten­tial for fur­ther research, along with help­ing to explain the incred­ible mor­pho­lo­gic­al diversity we observe in sculpin craniofa­cial bones.

Eli G. Cytryn­baum, Clayton M. Small, and Charles B. Kim­mel are all research­ers at the Uni­ver­sity of Ore­gon. The ori­gin­al paper is freely avail­able to read and down­load from Evol­u­tion Letters.