Evolution in the Dark: Darwin's Loss Without Selection

223 Pages·2017·10.596 MB·English

by  Horst Wilkens, Ulrike Strecker (auth.)

Horst Wilkens · Ulrike Strecker
Evolution
in the Dark
Darwin's Loss Without Selection
Evolution in the Dark
Horst Wilkens (cid:129) Ulrike Strecker
Evolution in the Dark
Darwin’s Loss Without Selection
HorstWilkens UlrikeStrecker
CentrumfürNaturkunde—Zoologisches CentrumfürNaturkunde—Zoologisches
Museum Museum
Universita¨tHamburg Universita¨tHamburg
Hamburg,Germany Hamburg,Germany
ISBN978-3-662-54510-2 ISBN978-3-662-54512-6 (eBook)
DOI10.1007/978-3-662-54512-6
LibraryofCongressControlNumber:2017941083
#Springer-VerlagGmbHGermany2017
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Acknowledgements
Annelore Kr€oger patiently prepared the voluminous graphic work. The partly
coloureddrawingswereproducedbyMonikaHa¨nel.ArnhildWoltmannconstantly
providedreadyassistanceandDetlefTeegewasresponsibleforkeepingthefishin
good condition for many years. We express our deepest thanks to all of them for
theircontinuousassistanceandengagement. TheAstyanax projecthas beenspon-
soredbytheDeutscheForschungsgemeinschaftsince1970.Aboveallwethankthe
Mexican people and authorities for their help and permits. If not differently
assigned,thephotosarebytheauthors.
v
Contents
1 EvolutionintheDark:Introduction. . . . . . . . . . . . . . . . . . . . . . . . . 1
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2 TheRoleofRudimentationinEvolution. . . .. . . . . .. . . . .. . . . . .. 3
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
3 DiversityandthePhylogeneticAgeofCaveSpecies. . . . . . . . . . . . . 13
3.1 MexicoandthePeri-CaribbeanIslands:AHotSpotofAquatic
CaveSpeciesDiversity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
3.2 StronglyEye-ReducedCaveSpecies. . . . . . . . . . . . . . . . . . . . . 16
3.3 LesserandVariablyEye-ReducedCaveSpecies. . . . . . . . . . . . 20
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
4 SurfaceandCavePopulationsofMexicanAstyanax. . . . . . . . . . . . . 37
4.1 AstyanaxSurfaceFish. . . . . .. . . . . . . . . . .. . . . . . . . . . . .. . . 38
4.2 AstyanaxCaveFish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
4.3 PhylogeographyandSpeciationofSurfaceandCaveAstyanax. . . 44
4.3.1 InvasionofSurfaceAstyanaxfromSouthAmerica
andOriginoftheCaveForms. . . .. . . . .. . . . .. . . . .. 44
4.3.2 MultipleOriginofCaveForms. . . . . . . . . . . . . . . . . . . 48
4.3.3 PopulationGeneticDiversityofCavePopulations. . . . . 49
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50
5 ComplexityofInterrelationshipBetweenAstyanaxCave
andSurfaceFish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
5.1 GeneralRemarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54
5.2 StronglyEye-andPigment-ReducedCavePopulations. . . . . . . . 54
5.2.1 Pacho´nCaveFish. . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
5.2.2 YerbanizCaveFish. . . . . . . . . . . . . . . . . . . . . . . . . . . 57
5.3 VariablyEye-andPigment-Reduced(VEP)CavePopulations. . . 58
5.3.1 MicosCaveFish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
5.3.2 ChicaCaveFish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
5.3.3 CaballoMoroCaveFish. . . . . . . . . . . . . . . . . . . . . . . 66
5.3.4 MolinoCaveFish. . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
5.4 RoleofIntrogressiveHybridization. . . . . . . . . . . . . . . . . . . . . . 68
5.5 SpeciationandTaxonomyofAstyanaxSurfaceandCaveFish. . . 70
vii
viii Contents
5.5.1 SurfaceFish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
5.5.2 CaveFish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74
6 RegressiveandConstructiveTraitsinAstyanaxSurface
andCaveFish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
6.1 GeneralRemarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80
6.2 ReproductiveBehaviour. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
6.3 SexDetermination. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84
6.4 AuditoryCapacities. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
6.5 LateralLineSystem. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
6.6 Taste. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91
6.7 Olfaction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94
6.8 FeedingBehaviourandFoodUptake. . . . . . . . . . . . . . . . . . . . . 94
6.9 MetabolicAdaptationtoPermanentorPeriodicLow
FoodSupply. .. . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . .. 98
6.10 OverallSleepandActivityPatterns. . . . . . . . . . . . . . . . . . . . . . 102
6.11 EggYolkContent. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . 104
6.12 AggressiveBehaviouralPatternsinAstyanax. . . . . . . . . . . . . . . 106
6.13 DorsalLightReaction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 112
6.14 PhototacticBehaviour. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 114
6.15 PinealOrgan. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 116
6.16 CircadianRhythm. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118
6.17 FrightReaction.. . . .. . . .. . . .. . . .. . . .. . .. . . .. . . .. . . .. 127
6.18 SchoolingandShoalingBehaviour. . . . . . . . . . . . . . . . . . . . . . 129
6.19 Scales. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132
6.20 Pigmentation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
6.20.1 Melanophores. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
6.20.2 BrownGene(Mc1r). . . . . . . . . . . . . . . . . . . . . . . . . . . 134
6.20.3 AlbinoGene(Oca2). . .. . . .. . . . .. . . . .. . . .. . . . .. 137
6.20.4 GuanineandCarotinoids. . . . . . . . . . . . . . . . . . . . . . . 138
6.21 Eye. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 140
6.21.1 MorphologyandHistologyoftheEyesoftheSurface
andtheSEPAstyanaxCaveFish. . . . . . . . . . . . . . . . . 140
6.21.2 VisualPigments. . .. . . . . . . . .. . . . . . . .. . . . . . . .. . 142
6.21.3 SizeandHistologyoftheEyeintheVEPCaveFish
andintheCrossingsBetweenSurfaceandCaveFish. . . 144
6.21.4 OntogenyofEyeDevelopmentintheSEPCaveFish. . . 148
6.21.5 GeneticBasisofEyeDevelopment. . . . . . . . . . . . . . . . 156
6.21.6 TheRoleoftheLensinEyeDevelopment. . . . . . . . . . 161
6.21.7 OntogeneticEyeRegressionandHeadFormation. . . . . 162
6.21.8 RootEffect. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165
6.22 Brain. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166
6.23 ComparisonoftheGeneticsofComplexRegressive
andConstructiveTraits. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169
Contents ix
6.23.1 PhenotypicManifestationandGeneExpression. . . . . . . 169
6.23.2 ComparisonofPhenotypicManifestation. . . . . . . . . . . 173
6.23.3 GeneticsofPhylogeneticallyYoungVEPCaveFish. . . 175
6.23.4 SignificanceofUnproportionalEpistaticGeneEffect. . . 177
6.23.5 NatureofGenesResponsibleforComplexTraits. . . . . . 178
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 179
7 MechanismsofRegressiveEvolution. . . . . . . . . . . . . . . . . . . . . . . . 191
7.1 DeleteriousRisk. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192
7.2 FoodLimitationandEnergyEconomy. . . . . . . . . . . . . . . . . . . . 192
7.3 QuantitativeTraitLociPolarityTestforSelection
(Orr’sSignTest). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193
7.4 Pleiotropy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194
7.4.1 PleiotropyofSonicHedgehog(Shh)Genes. . . . . . . . . . 194
7.4.2 PleiotropyofNeuromodulation(Melanin-Catecholamine
Trade-OffHypothesis). . . . . . . . . . . . . . . . . . . . . . . . . 195
7.4.3 PleiotropyofVibrationAttractionBehaviour(VAB)
andSuperficialNeuromastsintheCaveFishOrbit. . . . 197
7.5 IndependentInheritance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 198
7.6 EvolutionaryRatesofRegressiveandConstructiveTraits. . . . . . 199
7.7 ReversibilityofRegressiveEvolution. . . . . . . . . . . . . . . . . . . . 200
7.8 VariabilityandLoss:NeutralMutationTheory. . . . . . . . . . . . . 201
7.8.1 VariabilityofRegressiveTraits. . . . . . . . . . . . . . . . . . 203
7.8.2 LossofBehaviouralTraitsNotPerformedinDarkness. . . 205
7.8.3 GeneticStudies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205
7.9 VariabilityandConstructive(Darwin’s)Gain. . . . . .. . . . . . . .. 207
7.10 ConcludingRemarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 211
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 211
1
Evolution in the Dark: Introduction
Abstract
Evolutionispredominantlyunderstoodasaprogressiveprocess,andlessatten-
tionisusuallypaidtothosetraitsbeingreducedatthesametime.SinceDarwin,
whowasthefirsttoexpoundwhatcanbecalled‘Darwin’sloss’,themainagents
ofregressionhavebeenunderdispute.
Because evolution is considered to progress over time, the features that are con-
structively improved during adaptive development have been the main focus of
scientific research. Less attention has been paid to the fact that, at the same time,
other traits lose their function and are subjected to reduction and regressive
evolution. Two types of this, aphanisia and rudimentation, were proposed to
occur (Sewertzoff 1931). Aphanisia structures are those that have lost their
biological function at some stage during the species-specific individual life span,
such as larval tadpoles and tunicates losing their tails or insect larvae completely
reducing specific or even all body parts during metamorphosis. In contrast,
rudimentation characterizes the process of reduction of features that have lost
their biological function at all ontogenetic stages. Rudimentation develops either
whenatraithadlostitsbiologicalsignificanceorwhenitsfunctionisreplacedby
anotherone(Sewertzoff1931).Suchprocessesexceedtheindividuallifespanand
generally take thousands of years. Furthermore, rudimentation differs from
aphanisia by the long-lasting existence of intermediate transitional stages, which
mayshowhighvariability.
Whereasthereisnodoubtthatselectionplaysanimportantroleinconstructive
evolution,theunderlyingprocessesofrudimentationarestillunderdispute(Culver
and Wilkens 2000; Re´taux and Casane 2013). Darwin was already aware of this
problemwhenhestated“Thereremains,however,thisdifficulty:afteranorganhas
ceased being used, and has become in consequence much reduced, how can it be
stillfurtherreducedinsizeuntilthemerestvestigeisleft;andhowcanitbefinally
quiteobliterated?”Inthefaceoftheneodarwinianparadigmofselectionasanagent
#Springer-VerlagGmbHGermany2017 1
H.Wilkens,U.Strecker,EvolutionintheDark,DOI10.1007/978-3-662-54512-6_1
2 1 EvolutionintheDark:Introduction
exclusively applied to explain evolutionary processes in recent times, almost
countlesseffortshavebeenmadetoexplain‘Darwin’sloss’andtodetectselection,
whichisnolongerassumedtohavedirectinfluenceonrudimentation.Thisissueis
mostevidentincave-livingspecies,inwhich,inparticular,thelossoftheeyeshas
fascinated biologists since Darwin. Cave animals have become prime subjects to
study pheno- and genotypic principles, not only of regression but of evolution in
general.Theyprovideexceptionaltoolstostudytheprocessofevolutionfarbeyond
that of eye and pigment reduction. As a result of the close relationship to their
surface sister forms, cave species enable comparative morphological, physiologi-
cal, and behavioural analyses of regressive and constructive traits. Persisting
interfertilityoftenallowstheanalysisofthegeneticbasesanddifferencesbetween
surface and cave forms. Furthermore, in combination with paleobiogeography,
evolutionaryratesofconstructiveorregressivetraitsliketherudimentaryeyecan
becalculatedbasedonmolecularandmorphologicalanalyses.
References
Culver DC, Wilkens H (2000) Critical review of the relevant theories of the evolution of
subterranean animals. In: Wilkens H, Culver DC, Humphreys WF (eds) Ecosystems of the
world:subterraneanecosystems,vol30.Elsevier,Amsterdam,pp381–398
Re´tauxS,CasaneD(2013)Evolutionofeyedevelopmentinthedarknessofcaves:adaptation,
drift,orboth?EvoDevo4(1):1–12
SewertzoffAN(1931)MorphologischeGesetzma¨ßigkeitenderEvolution.Jena,Germany