Experimental evolution

File:Big and little dog 1.jpg mix and Great Dane show the wide range of dog breed sizes created using artificial selection.]]

Unwittingly, humans have carried out evolution experiments for as long as they have been domesticating plants and animals. Selective breeding of plants and animals has led to varieties that differ dramatically from their original wild-type ancestors. Examples are the cabbage varieties, maize, or the large number of different dog breeds. The power of human breeding to create varieties with extreme differences from a single species was already recognized by Charles Darwin. In fact, he started out his book The Origin of Species with a chapter on variation in domestic animals. In this chapter, Darwin discussed in particular the pigeon.

{{quotation|Altogether at least a score of pigeons might be chosen, which if shown to an ornithologist, and he were told that they were wild birds, would certainly, I think, be ranked by him as well-defined species. Moreover, I do not believe that any ornithologist would place the English carrier, the short-faced tumbler, the runt, the barb, pouter, and fantail in the same genus; more especially as in each of these breeds several truly-inherited sub-breeds, or species as he might have called them, could be shown him.

(...) I am fully convinced that the common opinion of naturalists is correct, namely, that all have descended from the rock-pigeon (Columba livia), including under this term several geographical races or sub-species, which differ from each other in the most trifling respects.|Charles Darwin|The Origin of Species}}

File:Dallinger Incubator J.R.Microscop.Soc.1887p193.png

One of the first to carry out a controlled evolution experiment was William Dallinger. In the late 19th century, he cultivated small unicellular organisms in a custom-built incubator over a time period of seven years (1880–1886). Dallinger slowly increased the temperature of the incubator from an initial 60 °F up to 158 °F. The early cultures had shown clear signs of distress at a temperature of 73 °F, and were certainly not capable of surviving at 158 °F. The organisms Dallinger had in his incubator at the end of the experiment, on the other hand, were perfectly fine at 158 °F. However, these organisms would no longer grow at the initial 60 °F. Dallinger concluded that he had found evidence for Darwinian adaptation in his incubator, and that the organisms had adapted to live in a high-temperature environment. Dallinger's incubator was accidentally destroyed in 1886, and Dallinger could not continue this line of research.{{cite journal | vauthors = Haas JW | title = The Reverend Dr William Henry Dallinger, F.R.S. (1839-1909) | journal = Notes and Records of the Royal Society of London | volume = 54 | issue = 1 | pages = 53–65 | date = January 2000 | pmid = 11624308 | doi = 10.1098/rsnr.2000.0096 | s2cid = 145758182 }}{{Cite book|chapter-url=https://ncse.ngo/files/pub/evolution/Excerpt--lightofevolution.pdf|chapter=Darwin Under the Microscope: Witnessing Evolution in Microbes| vauthors = Zimmer C |title=In the Light of Evolution: Essays from the Laboratory and Field|publisher=W. H. Freeman|year=2011|isbn=978-0-9815194-9-4| veditors = Losos J |pages=42–43}}

From the 1880s to 1980, experimental evolution was intermittently practiced by a variety of evolutionary biologists, including the highly influential Theodosius Dobzhansky. Like other experimental research in evolutionary biology during this period, much of this work lacked extensive replication and was carried out only for relatively short periods of evolutionary time.{{cite journal| vauthors = Dobzhansky T, Pavlovsky O |title=An experimental study of interaction between genetic drift and natural selection|journal=Evolution|date=1957|volume=11|issue=3|pages=311–319|doi=10.2307/2405795|jstor=2405795}}

Experimental evolution has been used in various formats to understand underlying evolutionary processes in a controlled system. Experimental evolution has been performed on multicellular{{cite journal | vauthors = Marden JH, Wolf MR, Weber KE | title = Aerial performance of Drosophila melanogaster from populations selected for upwind flight ability | journal = The Journal of Experimental Biology | volume = 200 | issue = Pt 21 | pages = 2747–2755 | date = November 1997 | pmid = 9418031 | doi = 10.1242/jeb.200.21.2747 }} and unicellular{{cite journal | vauthors = Ratcliff WC, Denison RF, Borrello M, Travisano M|author4-link=Michael Travisano | title = Experimental evolution of multicellularity | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 109 | issue = 5 | pages = 1595–1600 | date = January 2012 | pmid = 22307617 | pmc = 3277146 | doi = 10.1073/pnas.1115323109 | doi-access = free | bibcode = 2012PNAS..109.1595R }} eukaryotes, prokaryotes,{{cite journal | vauthors = Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim JF | display-authors = 6 | title = Genome evolution and adaptation in a long-term experiment with Escherichia coli | journal = Nature | volume = 461 | issue = 7268 | pages = 1243–1247 | date = October 2009 | pmid = 19838166 | doi = 10.1038/nature08480 | s2cid = 4330305 | bibcode = 2009Natur.461.1243B }} and viruses.{{cite journal | vauthors = Heineman RH, Molineux IJ, Bull JJ | title = Evolutionary robustness of an optimal phenotype: re-evolution of lysis in a bacteriophage deleted for its lysin gene | journal = Journal of Molecular Evolution | volume = 61 | issue = 2 | pages = 181–191 | date = August 2005 | pmid = 16096681 | doi = 10.1007/s00239-004-0304-4 | s2cid = 31230414 | bibcode = 2005JMolE..61..181H }} Similar works have also been performed by directed evolution of individual enzyme,{{cite journal | vauthors = Bloom JD, Arnold FH | title = In the light of directed evolution: pathways of adaptive protein evolution | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 106 | issue = Suppl 1 | pages = 9995–10000 | date = June 2009 | pmid = 19528653 | pmc = 2702793 | doi = 10.1073/pnas.0901522106 | doi-access = free }}{{cite journal | vauthors = Moses AM, Davidson AR | title = In vitro evolution goes deep | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 108 | issue = 20 | pages = 8071–8072 | date = May 2011 | pmid = 21551096 | pmc = 3100951 | doi = 10.1073/pnas.1104843108 | doi-access = free | bibcode = 2011PNAS..108.8071M }} ribozyme{{cite journal | vauthors = Salehi-Ashtiani K, Szostak JW | title = In vitro evolution suggests multiple origins for the hammerhead ribozyme | journal = Nature | volume = 414 | issue = 6859 | pages = 82–84 | date = November 2001 | pmid = 11689947 | doi = 10.1038/35102081 | s2cid = 4401483 | bibcode = 2001Natur.414...82S }} and replicator{{cite journal | vauthors = Sumper M, Luce R | title = Evidence for de novo production of self-replicating and environmentally adapted RNA structures by bacteriophage Qbeta replicase | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 72 | issue = 1 | pages = 162–166 | date = January 1975 | pmid = 1054493 | pmc = 432262 | doi = 10.1073/pnas.72.1.162 | doi-access = free | bibcode = 1975PNAS...72..162S }}{{cite journal | vauthors = Mills DR, Peterson RL, Spiegelman S | title = An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 58 | issue = 1 | pages = 217–224 | date = July 1967 | pmid = 5231602 | pmc = 335620 | doi = 10.1073/pnas.58.1.217 | doi-access = free | bibcode = 1967PNAS...58..217M }} genes.

File:Dysaphis anthrisci majkopica.gif

In the 1950s, the Soviet biologist Georgy Shaposhnikov conducted experiments on aphids of the Dysaphis genus. By transferring them to plants normally nearly or completely unsuitable for them, he had forced populations of parthenogenetic descendants to adapt to the new food source to the point of reproductive isolation from the regular populations of the same species.{{cite journal | vauthors = Shaposhnikov GK | title = Origin and breakdown of reproductive isolation and the criterion of the species. | journal = Entomological Review | date = 1966 | volume = 45 | pages = 1–8 | url = http://rogov.zwz.ru/Macroevolution/epi17.pdf | archive-url = https://web.archive.org/web/20130908054552/http://rogov.zwz.ru/Macroevolution/epi17.pdf | archive-date = 2013-09-08 }}

One of the first of a new wave of experiments using this strategy was the laboratory "evolutionary radiation" of Drosophila melanogaster populations that Michael R. Rose started in February, 1980.{{cite journal | vauthors = Rose MR | title = Artificial Selection on a Fitness-Component in Drosophila Melanogaster | journal = Evolution; International Journal of Organic Evolution | volume = 38 | issue = 3 | pages = 516–526 | date = May 1984 | pmid = 28555975 | doi = 10.2307/2408701 | jstor = 2408701 }} This system started with ten populations, five cultured at later ages, and five cultured at early ages. Since then more than 200 different populations have been created in this laboratory radiation, with selection targeting multiple characters. Some of these highly differentiated populations have also been selected "backward" or "in reverse," by returning experimental populations to their ancestral culture regime. Hundreds of people have worked with these populations over the better part of three decades. Much of this work is summarized in the papers collected in the book Methuselah Flies.{{Cite book|title=Methuselah Flies| vauthors = Rose MR, Passananti HB, Matos M |publisher=World Scientific |year=2004 |isbn=978-981-238-741-7|location=Singapore|doi=10.1142/5457}}

The early experiments in flies were limited to studying phenotypes but the molecular mechanisms, i.e., changes in DNA that facilitated such changes, could not be identified. This changed with genomics technology.{{cite journal | vauthors = Burke MK, Dunham JP, Shahrestani P, Thornton KR, Rose MR, Long AD | title = Genome-wide analysis of a long-term evolution experiment with Drosophila | journal = Nature | volume = 467 | issue = 7315 | pages = 587–590 | date = September 2010 | pmid = 20844486 | doi = 10.1038/nature09352 | bibcode = 2010Natur.467..587B | s2cid = 205222217 }} Subsequently, Thomas Turner coined the term Evolve and Resequence (E&R) and several studies used E&R approach with mixed success.{{cite journal | vauthors = Schlötterer C, Tobler R, Kofler R, Nolte V | title = Sequencing pools of individuals - mining genome-wide polymorphism data without big funding | journal = Nature Reviews. Genetics | volume = 15 | issue = 11 | pages = 749–763 | date = November 2014 | pmid = 25246196 | doi = 10.1038/nrg3803 | s2cid = 35827109 }}{{cite journal | vauthors = Schlötterer C, Kofler R, Versace E, Tobler R, Franssen SU | title = Combining experimental evolution with next-generation sequencing: a powerful tool to study adaptation from standing genetic variation | journal = Heredity | volume = 114 | issue = 5 | pages = 431–440 | date = May 2015 | pmid = 25269380 | pmc = 4815507 | doi = 10.1038/hdy.2014.86 }} One of the more interesting experimental evolution studies was conducted by Gabriel Haddad's group at UC San Diego, where Haddad and colleagues evolved flies to adapt to low oxygen environments, also known as hypoxia.{{cite journal | vauthors = Zhou D, Xue J, Chen J, Morcillo P, Lambert JD, White KP, Haddad GG | title = Experimental selection for Drosophila survival in extremely low O(2) environment | journal = PLOS ONE | volume = 2 | issue = 5 | pages = e490 | date = May 2007 | pmid = 17534440 | pmc = 1871610 | doi = 10.1371/journal.pone.0000490 | doi-access = free | bibcode = 2007PLoSO...2..490Z }} After 200 generations, they used E&R approach to identify genomic regions that were selected by natural selection in the hypoxia adapted flies.{{cite journal | vauthors = Zhou D, Udpa N, Gersten M, Visk DW, Bashir A, Xue J, Frazer KA, Posakony JW, Subramaniam S, Bafna V, Haddad GG | display-authors = 6 | title = Experimental selection of hypoxia-tolerant Drosophila melanogaster | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 108 | issue = 6 | pages = 2349–2354 | date = February 2011 | pmid = 21262834 | pmc = 3038716 | doi = 10.1073/pnas.1010643108 | doi-access = free | bibcode = 2011PNAS..108.2349Z }} More recent experiments are following up E&R predictions with RNAseq{{cite journal | vauthors = Remolina SC, Chang PL, Leips J, Nuzhdin SV, Hughes KA | title = Genomic basis of aging and life-history evolution in Drosophila melanogaster | journal = Evolution; International Journal of Organic Evolution | volume = 66 | issue = 11 | pages = 3390–3403 | date = November 2012 | pmid = 23106705 | pmc = 4539122 | doi = 10.1111/j.1558-5646.2012.01710.x }} and genetic crosses. Such efforts in combining E&R with experimental validations should be powerful in identifying genes that regulate adaptation in flies.

Much recently the experimental evolution in flies have taken the course to address the molecular mechanisms{{cite journal |last1=Shrivastava |first1=Nidhi Krishna |last2=Shakarad |first2=Mallikarjun N. |title=Correlated responses in basal immune function in response to selection for fast development in Drosophila melanogaster |journal=Journal of Evolutionary Biology |date=May 2023 |volume=36 |issue=5 |pages=816–828 |doi=10.1111/jeb.14176 |pmid=37073855 }}{{cite journal |last1=Shrivastava |first1=Nidhi Krishna |last2=Chauhan |first2=Namita |last3=Shakarad |first3=Mallikarjun N. |title=Heightened immune surveillance in Drosophila melanogaster populations selected for faster development and extended longevity |journal=Heliyon |date=December 2022 |volume=8 |issue=12 |pages=e12090 |doi=10.1016/j.heliyon.2022.e12090 |doi-access=free |pmid=36544838 |pmc=9761728 |bibcode=2022Heliy...812090S }} and in doing so it might pave way to understand physiology of an organism better and thus redefine disease therapeutics.{{cite journal |last1=Shrivastava |first1=Nidhi Krishna |last2=Farand |first2=Abhishek Kumar |last3=Shakarad |first3=Mallikarjun N. |title=Long-term selection for faster development and early reproduction leads to up-regulation of genes involved in redox homeostasis |journal=Advances in Redox Research |date=December 2022 |volume=6 |pages=100045 |doi=10.1016/j.arres.2022.100045 |doi-access=free }}

{{see also|Serial passage}}

Many microbial species have short generation times, easily sequenced genomes, and well-understood biology. They are therefore commonly used for experimental evolution studies. The bacterial species most commonly used for experimental evolution include P. fluorescens,{{cite journal | vauthors = Rainey PB, Travisano M | title = Adaptive radiation in a heterogeneous environment | journal = Nature | volume = 394 | issue = 6688 | pages = 69–72 | date = July 1998 | pmid = 9665128 | doi = 10.1038/27900 | s2cid = 40896184 | bibcode = 1998Natur.394...69R }} Pseudomonas aeruginosa,{{cite journal | vauthors = Chua SL, Ding Y, Liu Y, Cai Z, Zhou J, Swarup S, Drautz-Moses DI, Schuster SC, Kjelleberg S, Givskov M, Yang L | display-authors = 6 | title = Reactive oxygen species drive evolution of pro-biofilm variants in pathogens by modulating cyclic-di-GMP levels | journal = Open Biology | volume = 6 | issue = 11 | pages = 160162 | date = November 2016 | pmid = 27881736 | pmc = 5133437 | doi = 10.1098/rsob.160162 }} Enterococcus faecalis {{Cite journal| vauthors = Ma Y, Chua SL |date=2021-11-15|title=No collateral antibiotic sensitivity by alternating antibiotic pairs |journal=The Lancet Microbe|volume=3 |issue=1 |pages=e7 |language=English|doi=10.1016/S2666-5247(21)00270-6|pmid=35544116 |s2cid=244147577|issn=2666-5247|doi-access=free}} and E. coli (see below), while the Yeast S. cerevisiae has been used as a model for the study of eukaryotic evolution.{{cite journal | vauthors = Rainey PB, Travisano M | title = Adaptive radiation in a heterogeneous environment | journal = Nature | volume = 394 | issue = 6688 | pages = 69–72 | date = July 1998 | pmid = 9665128 | pmc = 3758440 | doi = 10.1038/nature12344 | bibcode = 2013Natur.500..571L }}

{{Main article|E. coli long-term evolution experiment}}

One of the most widely known examples of laboratory bacterial evolution is the long-term E.coli experiment of Richard Lenski. On February 24, 1988, Lenski started growing twelve lineages of E. coli under identical growth conditions.{{Cite journal| vauthors = Lenski RE, Rose MR, Simpson SC, Tadler SC |date=1991-12-01|title=Long-Term Experimental Evolution in Escherichia coli. I. Adaptation and Divergence During 2,000 Generations|journal=The American Naturalist|volume=138|issue=6|pages=1315–1341|doi=10.1086/285289|s2cid=83996233|issn=0003-0147}}{{cite journal | vauthors = Fox JW, Lenski RE | title = From Here to Eternity--The Theory and Practice of a Really Long Experiment | journal = PLOS Biology | volume = 13 | issue = 6 | pages = e1002185 | date = June 2015 | pmid = 26102073 | pmc = 4477892 | doi = 10.1371/journal.pbio.1002185 | doi-access = free }} When one of the populations evolved the ability to aerobically metabolize citrate from the growth medium and showed greatly increased growth,{{cite journal | vauthors = Blount ZD, Borland CZ, Lenski RE | title = Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 105 | issue = 23 | pages = 7899–7906 | date = June 2008 | pmid = 18524956 | pmc = 2430337 | doi = 10.1073/pnas.0803151105 | doi-access = free | bibcode = 2008PNAS..105.7899B }} this provided a dramatic observation of evolution in action. The experiment continues to this day, and is now the longest-running (in terms of generations) controlled evolution experiment ever undertaken.{{Citation needed|date=November 2016}} Since the inception of the experiment, the bacteria have grown for more than 60,000 generations. Lenski and colleagues regularly publish updates on the status of the experiments.{{cite web | url = http://myxo.css.msu.edu/ecoli/ | title = E. coli Long-term Experimental Evolution Project Site | vauthors = Lenski RE | publisher = Michigan State University | access-date = 2004-07-08 | archive-date = 2017-07-27 | archive-url = https://web.archive.org/web/20170727225642/http://myxo.css.msu.edu/ecoli/ | url-status = dead }}

Bussotti and collaborators isolated amastigotes from Leishmania donovani and cultured them in vitro for 3800 generations (36 weeks). The culture of these parasites showed how they adapted to in vitro conditions by compensating for the loss of a NIMA-related kinase, important for the correct progression of mitosis, by increasing the expression of another orthologous kinase as the culture generations progressed. Furthermore, it was observed how L. donovani has been adapted to in vitro culture by reducing the expression of 23 transcripts related to flagellar biogenesis and increasing the expression of ribosomal protein clusters and non-coding RNAs such as nucleolar small RNAs. Flagella are considered less necessary by the parasite in in vitro culture and therefore the progression of generations leads to their elimination, causing an energy saving due to lower motility so that proliferation and growth rate in culture is higher. The amplified snoRNAs also lead to increased ribosomal biosynthesis, increased protein biosynthesis and thus increased growth rate of the culture. These adaptations observed over generations of parasites are governed by copy number variations (CNV) and epistatic interactions between affected genes, and allow us to justify Leishmania genomic instability through its post-transcriptional regulation of gene expression.{{cite journal |last1=Bussotti |first1=Giovanni |last2=Piel |first2=Laura |last3=Pescher |first3=Pascale |last4=Domagalska |first4=Malgorzata A. |last5=Rajan |first5=K. Shanmugha |last6=Cohen-Chalamish |first6=Smadar |last7=Doniger |first7=Tirza |last8=Hiregange |first8=Disha-Gajanan |last9=Myler |first9=Peter J. |last10=Unger |first10=Ron |last11=Michaeli |first11=Shulamit |last12=Späth |first12=Gerald F. |title=Genome instability drives epistatic adaptation in the human pathogen Leishmania |journal=Proceedings of the National Academy of Sciences |date=21 December 2021 |volume=118 |issue=51 |pages=e2113744118 |doi=10.1073/pnas.2113744118 |pmid=34903666 |pmc=8713814 |bibcode=2021PNAS..11813744B |language=en |issn=0027-8424|doi-access=free }}

File:Wheel Counter Box 1.jpg

In 1993, Theodore Garland, Jr. and colleagues started a long-term experiment that involves selective breeding of mice for high voluntary activity levels on running wheels.{{cite journal |last1=Swallow |first1=John G. |last2=Carter |first2=Patrick A. |last3=Garland, Jr. |first3=Theodore |title=Artificial Selection for Increased Wheel-Running Behavior in House Mice |journal=Behavior Genetics |date=1998 |volume=28 |issue=3 |pages=227–237 |doi=10.1023/a:1021479331779 |pmid=9670598 }} This experiment also continues to this day (> 105 generations). Mice from the four replicate "High Runner" lines evolved to run almost three times as many running-wheel revolutions per day compared with the four unselected control lines of mice, mainly by running faster than the control mice rather than running for more minutes/day. However, the High Runner lines have evolved in somewhat different ways, with some emphasizing running speed versus duration or vice versa, thus demonstrating "multiple solutions"

{{cite journal

|last1=Garland, Jr. |first1=T.

|last2=Kelly |first2=S. A.

|last3=Malisch |first3=J. L.

|last4=Kolb |first4=E. M.

|last5=Hannon |first5=R. M.

|last6=Keeney |first6=B. K.

|last7=Van Cleave |first7= S. L.

|last8=Middleton |first8 = K. M.

|title=How to run far: multiple solutions and sex-specific responses to selective breeding for high voluntary activity levels

|journal=Proceedings of the Royal Society B: Biological Sciences

|date=2011 |volume=278 |issue=1705

|pages=574–581 |doi=10.1098/rspb.2010.1584 |pmid=20810439 |pmc=3025687 }}

that seem to be based partly in evolved muscle characteristics.{{cite journal

|last1=Castro |first1=A. A.

|last2=Garland, Jr. |first2=T.

|last3=Ahmed |first3=S.

|last4=Holt |first4=N. C.

|title=Trade-offs in muscle physiology in selectively bred High Runner mice

|journal=Journal of Experimental Biology

|date=2022 |volume=225 |issue=23

|pages=jeb244083

|doi=10.1242/jeb.244083 |pmid=36408738 |pmc=9789404 }}

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The HR mice have an elevated endurance running ability

{{cite journal

|last1=Meek |first1=T. E.

|last2=Lonquich |first2=B. P.

|last3=Hannon |first3=R. M.

|last4=Garland, Jr. |first4=T.

|title=Endurance capacity of mice selectively bred for high voluntary wheel running

|journal=Journal of Experimental Biology

|date=2009 |volume=212 |issue=18

|pages=2908–2917

|doi=10.1242/jeb.028886 |pmid=19717672 }}

and maximal aerobic capacity

{{cite journal

|last1=Schwartz |first1=N. E.

|last2=McNamara |first2=M. P.

|last3=Orozco |first3=J. M.

|last4=Rashid |first4=J. O.

|last5=Thai |first5=A. P.

|last6=Garland, Jr. |first6=T.

|title=Selective breeding for high voluntary exercise in mice increases maximal (V̇_O2,max) but not basal metabolic rate

|journal=Journal of Experimental Biology

|date=2023 |volume=226 |issue=15

|pages=jeb245256

|doi=10.1242/jeb.245256 |pmid=37439323 |doi-access=free }} when tested on a motorized treadmill. They also exhibit alterations in motivation and the reward system of the brain. Pharmacological studies point to alterations in dopamine function and the endocannabinoid system.{{cite journal | vauthors = Keeney BK, Raichlen DA, Meek TH, Wijeratne RS, Middleton KM, Gerdeman GL, Garland T | title = Differential response to a selective cannabinoid receptor antagonist (SR141716: rimonabant) in female mice from lines selectively bred for high voluntary wheel-running behaviour | journal = Behavioural Pharmacology | volume = 19 | issue = 8 | pages = 812–820 | date = December 2008 | pmid = 19020416 | doi = 10.1097/FBP.0b013e32831c3b6b | s2cid = 16215160 }} The High Runner lines have been proposed as a model to study human attention-deficit hyperactivity disorder (ADHD), and administration of Ritalin reduces their wheel running approximately to the levels of control mice.{{cite journal

|last1=Rhodes |first1=J. S.

|last2=Garland, Jr. |first2=T.

|title=Differential sensitivity to acute administration of Ritalin, apomorphine, SCH 23390, and raclopride in mice selectively bred for hyperactive wheel-running behavior

|journal=Psychopharmacology

|date=2003 |volume=167 |issue=3

|pages=242–250

|doi=10.1007/s00213-003-1399-9 |pmid=12669177 }}

In 2005 Paweł Koteja with Edyta Sadowska and colleagues from the Jagiellonian University (Poland) started a multidirectional selection on a non-laboratory rodent, the bank vole Myodes (= Clethrionomys) glareolus.{{cite journal | vauthors = Sadowska ET, Baliga-Klimczyk K, Chrzaścik KM, Koteja P | title = Laboratory model of adaptive radiation: a selection experiment in the bank vole | journal = Physiological and Biochemical Zoology | volume = 81 | issue = 5 | pages = 627–640 | year = 2008 | pmid = 18781839 | doi = 10.1086/590164 | s2cid = 20125314 }} The voles are selected for three distinct traits, which played important roles in the adaptive radiation of terrestrial vertebrates: high maximum rate of aerobic metabolism, predatory propensity, and herbivorous capability. Aerobic lines are selected for the maximum rate of oxygen consumption achieved during swimming at 38°C; Predatory lines – for a short time to catch live crickets; Herbivorous lines – for capability to maintain body mass when fed a low-quality diet “diluted” with dried, powdered grass. Four replicate lines are maintained for each of the three selection directions and another four as unselected Controls.

After approximately 20 generations of selective breeding, voles from the Aerobic lines evolved a 60% higher swim-induced metabolic rate than voles from the unselected Control lines. Although the selection protocol does not impose a thermoregulatory burden, both the basal metabolic rate and thermogenic capacity increased in the Aerobic lines.{{cite journal | vauthors = Sadowska ET, Stawski C, Rudolf A, Dheyongera G, Chrząścik KM, Baliga-Klimczyk K, Koteja P | title = Evolution of basal metabolic rate in bank voles from a multidirectional selection experiment | journal = Proceedings. Biological Sciences | volume = 282 | issue = 1806 | pages = 20150025 | date = May 2015 | pmid = 25876844 | pmc = 4426621 | doi = 10.1098/rspb.2015.0025 | doi-access = free }}{{cite journal | vauthors = Dheyongera G, Grzebyk K, Rudolf AM, Sadowska ET, Koteja P | title = The effect of chlorpyrifos on thermogenic capacity of bank voles selected for increased aerobic exercise metabolism | journal = Chemosphere | volume = 149 | pages = 383–390 | date = April 2016 | pmid = 26878110 | doi = 10.1016/j.chemosphere.2015.12.120 | bibcode = 2016Chmsp.149..383D }} Thus, the results have provided some support for the “aerobic capacity model” for the evolution of endothermy in mammals.

More than 85% of the Predatory voles capture the crickets, compared to only about 15% of unselected Control voles, and they catch the crickets faster. The increased predatory behavior is associated with a more proactive coping style (“personality”).{{cite journal | vauthors = Maiti U, Sadowska ET, ChrzĄścik KM, Koteja P | title = Experimental evolution of personality traits: open-field exploration in bank voles from a multidirectional selection experiment | journal = Current Zoology | volume = 65 | issue = 4 | pages = 375–384 | date = August 2019 | pmid = 31413710 | pmc = 6688576 | doi = 10.1093/cz/zoy068 | doi-access = free }}

During the test with low-quality diet, the Herbivorous voles lose approximately 2 grams less mass (approximately 10% of the original body mass) than the Control ones. The Herbivorous voles have an altered composition of the bacterial microbiome in their caecum.{{cite journal | vauthors = Kohl KD, Sadowska ET, Rudolf AM, Dearing MD, Koteja P | title = Experimental Evolution on a Wild Mammal Species Results in Modifications of Gut Microbial Communities | journal = Frontiers in Microbiology | volume = 7 | pages = 634 | year = 2016 | pmid = 27199960 | pmc = 4854874 | doi = 10.3389/fmicb.2016.00634 | doi-access = free }} Thus, the selection has resulted in evolution of the entire holobiome, and the experiment may offer a laboratory model of hologenome evolution.

Synthetic biology offers unique opportunities for experimental evolution, facilitating the interpretation of evolutionary changes by inserting genetic modules into host genomes and applying selection specifically targeting such modules. Synthetic biological circuits inserted into the genome of Escherichia coli{{cite journal | vauthors = Sleight SC, Bartley BA, Lieviant JA, Sauro HM | title = Designing and engineering evolutionary robust genetic circuits | journal = Journal of Biological Engineering | volume = 4 | pages = 12 | date = November 2010 | pmid = 21040586 | pmc = 2991278 | doi = 10.1186/1754-1611-4-12 | doi-access = free }} or the budding yeast Saccharomyces cerevisiae{{cite journal | vauthors = González C, Ray JC, Manhart M, Adams RM, Nevozhay D, Morozov AV, Balázsi G | title = Stress-response balance drives the evolution of a network module and its host genome | journal = Molecular Systems Biology | volume = 11 | issue = 8 | pages = 827 | date = August 2015 | pmid = 26324468 | pmc = 4562500 | doi = 10.15252/msb.20156185 | doi-access = free }} degrade (lose function) during laboratory evolution. With appropriate selection, mechanisms underlying the evolutionary regain of lost biological function can be studied.{{cite journal | vauthors = Kheir Gouda M, Manhart M, Balázsi G | title = Evolutionary regain of lost gene circuit function | journal = Proceedings of the National Academy of Sciences | volume = 116 | issue = 50 | pages = 25162–25171 | date = December 2019 | pmid = 31754027 | pmc = 6911209 | doi = 10.1073/pnas.1912257116 | doi-access = free | bibcode = 2019PNAS..11625162K }} Experimental evolution of mammalian cells harboring synthetic gene circuits{{cite journal | vauthors = Farquhar KS, Charlebois DA, Szenk M, Cohen J, Nevozhay D, Balázsi G | title = Role of network-mediated stochasticity in mammalian drug resistance | journal = Nature Communications | volume = 10 | issue = 1 | pages = 2766 | date = June 2019 | pmid = 31235692 | pmc = 6591227 | doi = 10.1038/s41467-019-10330-w | doi-access = free }} reveals the role of cellular heterogeneity in the evolution of drug resistance, with implications for chemotherapy resistance of cancer cells.

Stickleback fish have both marine and freshwater species, the freshwater species evolving since the last ice age. Freshwater species can survive colder temperatures. Scientists tested to see if they could reproduce this evolution of cold-tolerance by keeping marine sticklebacks in cold freshwater. It took the marine sticklebacks only three generations to evolve to match the 2.5 degree Celsius improvement in cold-tolerance found in wild freshwater sticklebacks.{{cite journal | vauthors = Barrett RD, Paccard A, Healy TM, Bergek S, Schulte PM, Schluter D, Rogers SM | title = Rapid evolution of cold tolerance in stickleback | journal = Proceedings. Biological Sciences | volume = 278 | issue = 1703 | pages = 233–238 | date = January 2011 | pmid = 20685715 | pmc = 3013383 | doi = 10.1098/rspb.2010.0923 }}

Microbial cells {{cite journal | vauthors = Dragosits M, Mattanovich D | title = Adaptive laboratory evolution -- principles and applications for biotechnology | journal = Microbial Cell Factories | volume = 12 | issue = 1 | pages = 64 | date = July 2013 | pmid = 23815749 | pmc = 3716822 | doi = 10.1186/1475-2859-12-64 | doi-access = free }} and recently mammalian cells {{cite journal | vauthors = Maralingannavar V, Parmar D, Pant T, Gadgil C, Panchagnula V, Gadgil M | title = CHO Cells adapted to inorganic phosphate limitation show higher growth and higher pyruvate carboxylase flux in phosphate replete conditions | journal = Biotechnology Progress | volume = 33 | issue = 3 | pages = 749–758 | date = May 2017 | pmid = 28220676 | doi = 10.1002/btpr.2450 | s2cid = 4048737 }} are evolved under nutrient limiting conditions to study their metabolic response and engineer cells for useful characteristics.

Because of their rapid generation times microbes offer an opportunity to study microevolution in the classroom. A number of exercises involving bacteria and yeast teach concepts ranging from the evolution of resistance{{cite journal | vauthors = Hyman P | title = Bacteriophage as instructional organisms in introductory biology labs | journal = Bacteriophage | volume = 4 | issue = 1 | pages = e27336 | date = January 2014 | pmid = 24478938 | pmc = 3895413 | doi = 10.4161/bact.27336 }} to the evolution of multicellularity.{{cite journal|title=A Novel Laboratory Activity for Teaching about the Evolution of Multicellularity|journal=The American Biology Teacher|volume=76|issue=2|year=2014|pages=81–87|issn=0002-7685|doi=10.1525/abt.2014.76.2.3| vauthors = Ratcliff WC, Raney A, Westreich S, Cotner S |s2cid=86079463}} With the advent of next-generation sequencing technology it has become possible for students to conduct an evolutionary experiment, sequence the evolved genomes, and to analyze and interpret the results.{{cite report |type=Preprint |last1=Mikheyev |first1=Alexander S |last2=Arora |first2=Jigyasa |title=Using experimental evolution and next-generation sequencing to teach bench and bioinformatic skills |date=9 September 2015 |doi=10.7287/peerj.preprints.1356v1 |doi-access=free }}

Laboratory synthetic evolution is also used to develop new phenotypes in organisms used for biomanufacturing. Natural mutations can be complemented with methods that directly generate phenotypic diversity. With yeast, the generation of new phenotypes can be accelerated by manipulation at the transcription level: by stochastically introducing artificial transcription factors, globally altering the transcription machinery, CRISPR interference and activation. Also with yeast, transposons, loxP sequences, and highly error-prone orthogonal DNAP-DNA plasmid pairs can be used to accelerate the generation of mutations.{{cite journal |last1=Wang |first1=Zhen |last2=Qi |first2=Xianni |last3=Ren |first3=Xinru |last4=Lin |first4=Yuping |last5=Zeng |first5=Fanli |last6=Wang |first6=Qinhong |title=Synthetic evolution of Saccharomyces cerevisiae for biomanufacturing: Approaches and applications |journal=mLife |date=February 2025 |volume=4 |issue=1 |pages=1–16 |doi=10.1002/mlf2.12167|pmc=11868838 }}

{{Div col|small=yes}}

• Artificial selection
• Bacteriophage experimental evolution
• Directed evolution
• Domestication
• Evolutionary biology
• Evolutionary physiology
• Genetics
• Genomics of domestication
• Laboratory experiments of speciation
• Quantitative genetics
• Selection limits
• Selective breeding
• Tame Silver Fox

{{Div col end}}

{{reflist}}

{{refbegin|30em}}

• {{cite journal | vauthors = Bennett AF | title = Experimental evolution and the Krogh principle: generating biological novelty for functional and genetic analyses | journal = Physiological and Biochemical Zoology | volume = 76 | issue = 1 | pages = 1–11 | year = 2003 | pmid = 12695982 | doi = 10.1086/374275 | s2cid = 9032244 | url = https://zenodo.org/record/1059074 }}
• {{cite journal | vauthors = Dallinger WH | title = The president's address. | journal = Journal of the Royal Microscopical Society | date = April 1887 | volume = 7 | issue = 2 | pages = 185–99 | doi = 10.1111/j.1365-2818.1887.tb01566.x }}
• {{cite book | vauthors = Garland Jr T | author-link1 = Theodore Garland, Jr. | date = 2003 | chapter = Selection experiments: an under-utilized tool in biomechanics and organismal biology. | pages = 23–56 | veditors = Bels VL, Gasc JP, Casinos A | title = Vertebrate biomechanics and evolution. | publisher = BIOS Scientific Publishers | location = Oxford, UK | chapter-url = http://www.biology.ucr.edu/people/faculty/Garland/Garland_2003.pdf | access-date = 2007-02-10 | archive-date = 2015-09-23 | archive-url = https://web.archive.org/web/20150923190230/http://www.biology.ucr.edu/people/faculty/Garland/Garland_2003.pdf | url-status = dead }}
• {{cite book | url = https://www.ucpress.edu/book/9780520261808/experimental-evolution | veditors = Garland Jr T, Rose MR | date = 2009 | title = Experimental evolution: concepts, methods, and applications of selection experiments. | publisher = University of California Press | location = Berkeley, California | isbn = 978-0-520-26180-8 }}
• {{cite journal | vauthors = Gibbs AG | title = Laboratory selection for the comparative physiologist | journal = The Journal of Experimental Biology | volume = 202 | issue = Pt 20 | pages = 2709–2718 | date = October 1999 | pmid = 10504307 | doi = 10.1242/jeb.202.20.2709 }}
• {{cite book |doi=10.1002/9780470650288.ch8 |chapter=Phenotypic and Genomic Evolution during a 20,000-Generation Experiment with the Bacterium Escherichia coli |title=Plant Breeding Reviews |date=2003 |last1=Lenski |first1=Richard E. |pages=225–265 |isbn=978-0-471-46892-9 }}
• {{cite journal | vauthors = Lenski RE, Rose MR, Simpson SC, Tadler SC | year = 1991 | title = Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations | journal = American Naturalist | volume = 138 | issue = 6| pages = 1315–1341 | doi=10.1086/285289| s2cid = 83996233 }}
• {{cite journal | vauthors = McKenzie JA, Batterham P | title = The genetic, molecular and phenotypic consequences of selection for insecticide resistance | journal = Trends in Ecology & Evolution | volume = 9 | issue = 5 | pages = 166–169 | date = May 1994 | pmid = 21236810 | doi = 10.1016/0169-5347(94)90079-5 | bibcode = 1994TEcoE...9..166M }}
• {{cite journal | vauthors = Reznick DN, Bryant MJ, Roff D, Ghalambor CK, Ghalambor DE | title = Effect of extrinsic mortality on the evolution of senescence in guppies | journal = Nature | volume = 431 | issue = 7012 | pages = 1095–1099 | date = October 2004 | pmid = 15510147 | doi = 10.1038/nature02936 | s2cid = 205210169 | bibcode = 2004Natur.431.1095R }}
• {{cite book | veditors = Rose MR, Passananti HB, Matos M | date = 2004 | title = Methuselah flies: A case study in the evolution of aging. | publisher = World Scientific Publishing | location = Singapore }}
• {{cite journal | vauthors = Swallow JG, Garland T | title = Selection Experiments as a Tool in Evolutionary and Comparative Physiology: Insights into Complex Traits--an Introduction to the Symposium | journal = Integrative and Comparative Biology | volume = 45 | issue = 3 | pages = 387–390 | date = June 2005 | pmid = 21676784 | doi = 10.1093/icb/45.3.387 | author-link2 = Theodore Garland, Jr. | s2cid = 2305227 | doi-access = free }}

{{refend}}

• [http://myxo.css.msu.edu/ecoli/ E. coli Long-term Experimental Evolution Project Site] {{Webarchive|url=https://web.archive.org/web/20170727225642/http://myxo.css.msu.edu/ecoli/ |date=2017-07-27 }}, Lenski lab, Michigan State University
• A [http://www.biology.ucr.edu/people/faculty/Garland/Girard01.mov movie] illustrating the dramatic differences in wheel-running behavior.
• [https://sites.google.com/ucr.edu/hrmice/publications Experimental Evolution Publications by Ted Garland: Artificial Selection for High Voluntary Wheel-Running Behavior in House Mice] — a detailed list of publications.
• [http://biology.ucr.edu/people/faculty/Garland/ExperimentalEvolution.html Experimental Evolution] — a list of laboratories that study experimental evolution.
• [http://nere.bio.uci.edu/ Network for Experimental Research on Evolution], University of California.
• {{cite news |last1=Nicholls |first1=Henry |title=My little zebra: The secrets of domestication |url=https://www.newscientist.com/article/mg20427281-500-my-little-zebra-the-secrets-of-domestication/ |work=New Scientist |date=30 September 2009 }}
• Inquiry-based [https://biol.ucr.edu/idea/born_to_run/Born_to_Run.html middle school lesson plan: "Born to Run: Artificial Selection Lab"]
• [http://avida-ed.msu.edu/ Digital Evolution for Education software]

Category:Evolutionary biology

Category:Biology experiments