Evolution After Darwin

BIOLOGY & MEDICINE_Evolutionary Biology

Evolution after Darwin

Darwin’s pioneering work On the Origin of Species, in which he first formulated the principles of his theory of evolution, was published 150 years ago. This theory changed the thinking in biology significantly and influenced almost all areas of biological research. What could be more appropriate, then, than to stage a Max Planck Symposium on Evolutionary Biology in the Darwin Year 2009.

TEXT CHRISTINA BECK

volution goes on all the time.” Lenski’s studies began with twelve It was only after 33,000 generations This is the credo of Richard E. identical populations of an E. coli that a variant (Cit+) capable of exploit- Lenski of Michigan State Uni- strain. His objective was to find out ing citrate emerged – a fitness advan- versity. The American scientist whether random mutations that oc- tage that resulted in a clear increase in tracks evolution in the labora- curred in the past facilitate the evolu- the size of the population. So was this Etory with his team: some 21 years ago tion of key innovations. an extremely rare mutation, which he embarked on a long-term experi- would explain why its arrival was so ment with E. coli. Bacteria provide BILLIONS OF MUTATIONS delayed? Or was it a simple mutation good conditions for such experi- that had to be preceded by other muta- ments, as a bacterial population grows “One of the big advantages is that you tions in order for it to be phenotypical- to billions of cells within a very short can freeze bacteria and in this way ob- ly effective? “We tested these hypothe- time. Studying evolution in action tain fossil images,” explains the biolo- ses in experiments in which we calls for large numbers – it’s like play- gist. The bacteria grew on a medium repeated the evolution from different ing dice: if you roll the dice a hundred with a limited supply of glucose, starting points in the population his- times, you will almost certainly get a which also contained citrate. Howev- tory,” explained Lenski. six. Lenski hopes to overcome coinci- er, E. coli cannot use this citrate as a Not a single Cit+ mutant occurred dence through the sheer volume of source of carbon under oxygen condi- among the ten trillion ancestor cells cells and generations alone (“Our lab tions. “In the course of 30,000 gener- in the repeat experiments, either. All has produced 45,000 generations of ations, not a single generation devel- 19 Cit+ mutants obtained by the sci- bacteria so far”). His ultimate aim is to oped the ability to exploit citrates, entists originated from later clones. A identify the events that result in the even though each population had bil- sequence comparison of Cit+ and Cit advent of something new and original lions of mutations,” said Lenski. mutants showed that the necessary ci- in evolution. trate transporter was generated only

66 MaxPlanckResearch 3 | 09 The research studies presented at the Max Planck Symposium on Evolutionary Biology examined very different animal species including the beach mouse, which is a native of the US, cichlids from east Africa, the European great tit, and primates, including chimpanzees and us humans (l-r).

when the corresponding gene was Hopi Hoekstra from Harvard Univer- to their conspecifics inland, they have able to recruit a promoter – the start sity in her lecture “From Mice to Mol- lighter-colored and significantly re- sequence that made it possible to read ecules.” Convergence is a fascinating duced coat pigmentation on their fac- it in the first place. And this, in turn, phenomenon in evolution: unrelated es, flanks and tails. The fact that the had become possible only as a result species develop similar characteristics lighter-colored coat provides better of the duplication of another gene. or a similar appearance in response to camouflage in the sand dunes was The evolution of this phenotype was similar selection pressures. But does demonstrated by a simple experiment thus dependent on the population’s this phenotypic convergence imply in which the researchers placed a fake “genetic history.” genetic convergence? In other words: dark mouse coat in the dunes: it was Are the same genes actually responsi- immediately carried off and then later HOW MICE ACQUIRE A ble for the development of similar abandoned by a predator (probably an DIFFERENT COAT COLOR forms and patterns? To find out, owl or a hawk) when it realized it had Hoekstra and her team studied coat been tricked. Genetic research provides the strong- color variants in natural mouse popu- “At least three genes – Mc1r, Agou- est proof of evolutionary theory to- lations. ti and Corin – influence coat color,” re- day. Charles Darwin could not have The mouse species Peromyscus po- ported Hoekstra. The Melanocortin-1 even guessed at such things. Indeed, lionotus populates fallow fields in the receptor, Mc1r for short, plays a key the door to a more profound under- southeastern US. However, popula- role here in that it controls whether standing of evolution opened only tions are also found in the bright sand the dark pigment eumelanin or the when James Watson and Francis Crick dunes along the Gulf coast and more light pigment pheomelanin is pro- succeeded in decoding DNA in 1953. than 300 kilometers away on the At- duced. The researcher succeeded in “What can genes tell us about evolu- lantic coast near Florida. They are demonstrating that the exchange of a

Photos: Joel Sartore – Joelsartore.com/Vincent Musi/iStockphoto (2) tionary adaptation processes?” asked known as beach mice and, compared single nucleotide (a T instead of a C) in

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left The coffee breaks provided an opportunity for lively conversation and exchange, as seen here between Dieter Ebert from the University of Basle (center) and David G. Heckel from the Max Planck Institute for Chemical Ecology. right In her lecture “From Mice to Molecules,” Hopi Hoekstra explained the genetic mechanisms that control adaptations in the coat color of beach mice.

the sequence of the receptor gene in Using the Galapagos finches, Darwin been thought. Natural selection, that the mouse population originating had already clearly demonstrated the apparently endlessly cumbersome and from the Gulf coast altered the effec- fact that patterns, colors and forms slow mechanism of evolution, can tiveness of the receptor and hence can change as a result of evolution- clearly create new conditions within a changed the coat color. Arginine is ary adaptation processes. His draw- single generation. now inserted in position 65 in the ami- ings on this topic can still be found In another exciting finding, the re- no acid chain instead of cystein, and in every school science textbook to- searcher couple discovered that a new- this alters both the bonding of ligands day, and show how the finches devel- ly migrated larger species of bird could and the potential of the receptor for oped a thick beak for biting seeds, a make better use of the thicker seeds signal transmission. “Such Mc1r muta- longer and sharper one for flowers, than the long-established birds. The tions have also been observed in mam- and a short, pointed beak to access established residents responded to the moths,” added Hoekstra. tiny insects in rock crevices. As the arrival of the new competition through famous naturalist wrote in his travel adaptation – in precisely the opposite WHY DARWIN’S FINCHES APPEAR report of 1839: “Seeing this grada- direction as before, in that they now IN EVERY TEXTBOOK tion and diversity of structure in one developed smaller beaks. This meant small, intimately related group of they could access food sources in rock Interestingly, the lighter-colored coat birds, one might really fancy that crevices, for example, which their in the mice from the Atlantic coast from an original paucity of birds in thick-beaked rivals could not reach. could not be explained by the same this archipelago, one species had This adaptation, too, was quantifiable allele – the latter did not occur in been taken and modified for differ- in one generation of the birds. The re- them at all, nor could the researchers ent ends.” searchers call this phenomenon mi- find any new mutations in the Mc1r Rosemary and Peter Grant from croevolution. gene that would have influenced the Princeton succeeded in demonstrat- activity of the receptor. “Our findings ing the effect of natural selection di- HOW GREAT TITS FOLLOW show that a pigmentation pattern rectly. They studied the beaks of CLIMATE CHANGE that arose convergently in different ground finches on the island of mice populations that actually devel- Daphne Major and, at the same time, Other mechanisms also exist that oped under very similar conditions is recorded their food sources. In years could be the result of adaptation proc- clearly the result of completely differ- of extreme drought, a large part of the esses. Based on a long-term study car- ent genetic mechanisms,” said Hoek- population died and only the finches ried out in the UK, Ben Sheldon from stra. So there are different molecular with larger beaks survived because the University of Oxford demonstrat- solutions for attaining the same phe- they could crack thicker and harder ed that great tits are so plastic, in oth- notype under comparable environ- seeds when the seeds they usually fed er words adaptable, in their behavior mental conditions. The combination on became scarce. The beak shape is that the population as a whole is suc- of different alleles of the aforemen- not only inherited, as the Grants dis- cessfully adapting to the rapidly tioned genes Mc1r, Agouti and Corin covered. It also becomes established emerging changes in the climate. The may well play a role here. as an adaptation far faster than had researchers observed the breeding be-

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havior of the great tits in Wytham, a 375-hectare wooded area near Oxford, for five decades. No other bird population had been observed on an ongo- ing basis in a single location for such an extensive period. Between 1947 and 2009, the time of egg deposition shifted forward by around 14 days. “All of the data would indicate a close link between the average time of egg deposition in the population and the temperature that pre- vails in the period leading up to it,” explained Sheldon. Temperatures in spring – that is, before egg deposition – have increased markedly since the mid-1970s. Over the same period, the time window in which the majority of winter-moth grubs hatch has also moved forward. “The correlation between temperature and mating time is the same,” says Sheldon. The grubs are a key resource for the great tits, and the success of their breeding is largely dependent on the presence of these insects. Correct timing is im- portant for breeding and the selection pressure on the timing of egg ticity,” stressed Sheldon. The British develop and control brain function, deposition is high. The synchroniza- scientist also referred to “phenody- and therefore make behavioral reac- tion between egg deposition and the namics” in this context. tions possible in the first place. There peak in the hatching of the grubs is Russell D. Fernald of Stanford Uni- are growing indications that informa- maintained through the process’s versity proposed a bridge between tion generated in the social context close linkage with spring tempera- genes and behavior in his lecture. Al- can alter gene expression in the brain, tures. “And this would suggest that though genes do not directly specify and therefore also behavior. In order this adaptation is achieved solely the behavior of an organism, they to find out how social information is

Photos: Norbert Michalke through individual phenotypic plas- code for the molecular products that translated into cellular and molecular

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changes, the researchers looked for a es in behavior – that is, whether the Park, who had her first offspring at the corresponding model system. A spe- animals were aggressive or not – arose age of 13 and gave birth to subsequent cies of cichlid from Lake Tanganyika within a matter of minutes,” reported offspring at intervals of four to five in east Africa proved a lucky find: Fer- the American scientist. years and died at the young age of 45. nald and his colleagues were able to The changes in the brain were par- use it to demonstrate the influence of ticularly impressive: the gonadotro- EARLY WEANING OFFERS social interaction on the brain. pin-releasing hormone controls the ADVANTAGES release of gonadotropins and thus the SOCIAL CLIMBING GOES growth of the gonads. In T males, the A slide presented by Haig highlighted STRAIGHT TO THEIR HEADS GnRH-releasing neurons are eight the central observation deduced from times larger than they are in NT this: early weaning is a feature that is There are two different types of adult males. When a male was elevated specific to the human lifecycle. Hu- male cichlids: those that have a terri- from NT status to T status, the neuron man children are weaned at two to tory (T) and those with no territory size changed within a day and had three years of age, while chimpanzee (NT). Territorial males defend their reached the typical size of the GnRH- young remain at their mothers’ breast territory and are extremely aggressive releasing neurons of T males in less for an average of five years, and even toward neighboring males. They scare than a week. The researchers also re- as long as seven to eight years in the off non-territorial males and court the corded an increase in the GnRH mes- case of the Orangutan. This change in females, with whom they eventually senger RNA and the corresponding the course of the evolution of human mate. In contrast, between 70 and 90 protein. Conversely, the volume of children is based on reliable access to percent of NT males do not reproduce links between these neurons declined “supplementary” nutrition. “This re- at all. Their gonads are thus small in with loss of status – in other words, sults in childhood in humans includ- comparison with those of the T males. when a T male was transformed into ing an extended juvenile phase in They also lack the dark stripe on their an NT male. “The social behavior ac- which the offspring are weaned but heads and dots on the anal fin. These tually alters the brain in real time,” still dependent on their parents for dots look like eggs to the females. In explained Fernald in summary. their nutrition,” said Haig. Early wean- their attempts to gather them up, David Haig threw light on a com- ing is advantageous to the mother as they collect the seminal fluid of the T pletely different link between genes she is required to invest less of her own male, thus ensuring fertilization. and behavior. The researcher from resources (in the form of mother’s “What is exciting about this,” said Harvard University compared, first, milk) in rearing the young. Fernald, “is that this phenotypic state the reproductive history of two indi- Haig expects to gain a deeper in- can be completely reversed.” When viduals: a young woman who gave sight into this mother-child relation- the researchers placed NT males in a birth to her first child in her early 20s, ship through the study of genomic pool with smaller conspecifics, they bore additional children at intervals of imprinting and its effects. The follow- became T males. Conversely, T males two years, and eventually died at the ing phenomenon lies behind this: in a community with bigger territorial ripe old age of 80, and the female two copies of each gene are found in

males became NT males. “The chang- chimpanzee Fifi from Gombe National the fertilized ovum – one originating Photos: Norbert Michalke

70 MaxPlanckResearch 3 | 09 3 1 Hopi Hoekstra, Harvard University 2 Richard E. Lenski, Michigan State University 3 Ben Sheldon, Oxford University 4 45 Russel D. Fernald, Stanford University 5 David Haig, Harvard University

from the mother and the other from of their further development, the chil- the father. Imprinted genes are genes dren become obese, while simultane- GLOSSARY in which different effects arise de- ously suffering from delayed growth. Mutant pending on whether the maternal or A bacterial cell in which a genetic paternal allele is read. And it may well WHAT LIES BEHIND GENOMIC modification has occurred. be that there is a parental conflict at IMPRINTING? Clone work here: the paternal genes are gen- A population of bacterial cells whose erally less related than the maternal This phenotype confirms the theory phenotype is identical. genes to the fetuses arising from sub- according to which the expression of Phenotype sequent pregnancies – since, unlike the paternal gene should strengthen The overall appearance of an organism, the mother, the father is not always the appetite of the offspring in the the sum of its characteristics. the same. Therefore, according to phase in which they are fed exclusive- Ligand Haig’s hypothesis, the paternal genes ly on breast milk. However, the ques- A substance that can bind to a target protein, such as a receptor. try to mobilize more of the mother’s tion that arises here is whether the resources for the current fetus. The re- theory can also explain the change in Allele Different expressions of a gene generated searchers thus presume that imprint- the appetite in the course of the fur- through minor variations in the base ing developed at the genetic loci at ther development of PWS patients. sequence. which either the paternal or maternal The expression of paternal genes Inclusive fitness inclusive fitness is maximized through should obviously inhibit the child’s The optimization of the passing on of the extent of genetic expression. appetite for replacement nutrition. an organism’s own genes. Haig speculates as to the reasons for MISSING GENE COPY this: milk could be the more nutri- AFFECTS APPETITE tious or immunologically more valua- ble nutrition. Moreover, a longer nurs- With a view to testing these ideas, ing phase may well delay the birth of a David Haig examined the genetic con- younger sibling. In both cases, the dition Prader-Willi Syndrome in de- child that is already born benefits. tail. Subjects with this disorder lack “The study of imprinted genes in hu- the paternal copy of a gene that is im- mans can thus shed light on the rela- printed, or switched off, on the mater- tional interactions in our evolutionary nal side, with interesting effects: in the past,” stressed Haig in conclusion. immediate aftermath of their birth, As the famous geneticist and evolu- babies with PWS have little appetite tionary biologist Theodor Dobzhansky and little inclination to nurse. Within said: “Nothing in biology makes sense the first two years of their lives, how- except in the light of evolution.” This ever, they develop an insatiable appe- was impressively confirmed in the 14 tite for food. As a result, in the course lectures presented at this symposium.

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