Chapman et al., 2000), amphibians (Calhoon and …...Twenty weeks of living in the absence of light...

Animal Biology Vol 54 No 2 pp 137-158 (2004) Koninklijke Brill NV Leiden 2004Also available online - wwwbrillnl

Phenotypic plasticity its role in trophic radiation andexplosive speciation in cichlids (Teleostei Cichlidae)

JAY R STAUFFER JR lowast ELLEN VAN SNIK GRAY

School of Forest Resources Pennsylvania State University 12 Ferguson Building University ParkPA 16802 USA

AbstractmdashPhenotypic plasticity is the capacity of an organismrsquos phenotype to vary in differentenvironments Although diet-induced phenotypic plasticity has been documented in New Worldcichlids it has been hypothesised that this type of plasticity would be limited in certain Old Worldcichlids because of the morphological constraints on the jaw imposed by mouth-brooding Thishypothesis was experimentally tested by determining the effect of different diets on the head andjaw morphology of split broods of several species of haplochromine cichlids from Lake MalawiAfrica and two substrate-spawning cichlids one from the Old World Tilapia mariae (Boulenger)and one from the New World Herichthys cyanoguttatum (Baird and Girard) Different feeding regimesresulted in differences in head morphologies in both New and Old World cichlid species AlthoughOld World mouth-brooding haplochromine cichlids exhibited phenotypic plasticity the magnitudeof head-shape plasticity observed was greater in the New World substrate-spawning cichlid Hcyanoguttatum The Old World tilapiine cichlid T mariae did not exhibit phenotypic plasticity ofhead morphology Experiments with modified foods demonstrated that the observed changes wereunrelated to dietary nutrition but were a result of differing feeding modes Phenotypic plasticitymight have contributed to the extensive trophic radiation and subsequent explosive speciation observedin Old World haplochromine cichlids The existence of phenotypic plasticity has implications formorphology-based species descriptions as well

Keywords cichlids phenotypic plasticity speciation trophic polymorphism

INTRODUCTION

Phenotypic plasticity is defined as environmental modification of the phenotype(Bradshaw 1965) and has been documented in a wide range of organismsincluding fishes (Barlow 1961 Behnke 1972 Chernoff 1982 Meyer 1987Chapman et al 2000) amphibians (Calhoon and Jameson 1970 Newman 1988)

lowastCorresponding author e-mail vc5psuedu

138 JR Stauffer Jr E van Snik Gray

reptiles (Legler 1981) birds (James 1983) mammals (Williams and Moore1989) insects (Atchley 1971) and plants (Bradshaw 1965 Schlichting 1986)Two types of phenotypic plasticity developmental conversion and phenotypicmodulation can be characterised by direction and magnitude respectively (Smith-Gill 1983) Developmental conversion results in discrete morphs in response to anenvironmental cue (Stearns 1989 West-Eberhard 1989) Levins (1968) postulatedthat such conversions can be controlled by developmental switches or controllersthat determine attributes For example gender in turtles is determined by incubationtemperature Such switches can be non-plastic and under strict allelic control (Mayr1963) In contrast phenotypic modulations or reaction norms result in continuousvariation of a particular trait in response to an environmental stimulus (Woltereck1909 Stearns 1989) The direction and magnitude of phenotypic modulation maybe similar or different for related species (Schlichting 1986) The plasticity of thetrait itself is affected by natural selection and as such is under genetic control(Bradshaw 1965 West-Eberhard 1989) thus a given reaction norm may havea distinct evolutionary trajectory different from the plasticity with which it isassociated (Schlichting and Levin 1986)

The Great Lakes of Africa including lakes Malawi Tanganyika and Victoriaharbour the most speciose ichthyofauna of any of the worldrsquos lakes (Fryer and Iles1972 Kocher et al 1993) The endemic haplochromine cichlid fishes provide oneof the best examples of explosive vertebrate speciation Despite the morphologicalplasticity which has been observed in other fishes due to such environmental factorsas diet (Meyer 1987) temperature (Stearns 1989 Page and Burr 1991) light(Witte et al 1990) and predation pressure (Witte et al 1990) some authors haveassumed the morphology of African cichlid fishes to be developmentally canalised(van Oijen 1982)

Observed morphological variability observed in the Cichlidae may be due in partto phenotypic plasticity (Hoogerhoud 1984 Meyer 1987 1990a 1990b Witte et al1990 Wimberger 1991 1992) Witte (1984) hypothesised that differences in pre-maxilla development in wild-caught vs aquarium-raised Haplochromis squamipin-nis Regan from Lake George were due to differences in diet Hoogerhoud (1984)noted diet-dependent differences in the pharyngeal jaw apparatus of Gaurochromisand Labrochromis to be of the same magnitude as differences between these twogenera Furthermore the phenotypic divergence of the pharyngeal apparatus of theNew World Herichthys minckleyi (Kornfield and Taylor 1983) exceeds that ob-served among species of molluscivorous cichlids inhabiting Lake Victoria (Hooger-houd 1984) Differences in bone structure of the lower pharyngeal jaw associatedwith Astateroeochromis alluadi Pellegrin that were fed different diets were noted(Huysseune et al 1994 Smits et al 1996a b)

Meyer (1987) and Winberger 1991 1992) have directly tested the effects ofdiet on phenotypic plasticity in New World cichlids In general cichlid speciesthat feed by biting tend to have a short blunt (obtusorostral) snout whereasspecies that rely heavily on suction have a long pointed (acutorostral) snout (Barel

Phenotypic plasticity and cichlid speciation 139

1983) Meyer (1987) examined the effect of diet on the head morphology ofHerichthys managuense (Guumlnther) Meyer (1987) fed full siblings two differentdiets for 85 months and then quantified head shape Those individuals fed flakefood and oligochaetes developed a short blunt (obtusorostral) snout whereasthose individuals fed brine shrimp naupli developed a long pointed (acutorostral)snout The feeding regimes were then reversed for 85 months Those individualsthat had a short blunt snout converged to the long pointed snout form (Meyer1987) however the acutorostral form did not converge to the obtusorostral formMeyer (1987) concluded that a diet of flake food and oligochaetes at early agesdelayed ontogenetic transformation to the adult phenotype Meyer (1987) howeverhypothesised that the plasticity of mouth-brooding Old World cichlids may notbe as pronounced due to constraints on the jaw morphology for mouth broodingthus surrounding morphological structures may prevent a plastic structure fromresponding to its environment (Witte et al 1990) Furthermore free-swimmingsubstrate-spawning fry which feed at a younger age are smaller than mouth-brooding fry Because bone remodels less with age (Hinton and McNamara 1984)substrate-spawning fry were predicted to be more plastic than mouth-broodingfry (Wimberger 1991) thus any changes in head morphology of mouth-broodingjuveniles that occur before feeding commenced could be maladaptive (Wimberger1991)

Two species of Geophagus were selected by Wimberger (1991 1992) to examinethe magnitude of plasticity in mouth-brooding vs substrate-spawning New Worldcichlids Both species of Geophagus followed the expected trend with those fishraised on flake food having a short blunt snout and those fish raised on livebrine shrimp having long pointed snouts (Wimberger 1991) In a preliminarystudy F1 siblings derived from wild-caught Metriaclima pyrosontos StaufferBowers Kellogg and McKaye from Lake Malawi were randomly divided intotwo groups Stauffer et al (1995) fed one group flake food and the other brineshrimp naupli The two groups developed different head shapes after 18 weeks(Stauffer et al 1995) Based on these studies it appeared that mouth broodingmay not suppress the phenotypic plasticity induced by diet in either New Worldor Old World cichlids Witte (1984) reported that wild-caught and laboratory-reared Haplochromis squamipinnis Regan had differently shaped premaxillariesLaboratory-reared individuals of this Lake Victoria species frequently dug in thesand for food increasing the power of their bite Wild H squamipinnis do notexhibit this digging behaviour but are piscivores feeding by sucking fish from thewater column Furthermore the change in premaxillary shape was not restricted tojuveniles indicating that the plasticity was not limited by some ontogenetic factor(Witte 1984) Greenwood (1965) reported that the pharyngeal jaw apparatus of theOld World cichlid A alluadi is plastic Individuals feeding on thick-shelled snailshad stronger pharyngeal bones with larger molariform teeth than those feeding onthinner-shelled snails Twenty weeks of living in the absence of light resulted in


changes in the ocular structures of the Old World cichlid Oreochromis mossambicus(Peters) (Witte et al 1990)

Only one study has documented phenotypic plasticity in situ for Old Worldcichlids A significant decrease in the body depth and size of the Lake Victoriacichlid Haplochromis piceatus Greenwood and Gee was documented in the 1980s(Witte et al 1990) Dwarfed specimens (smaller individuals caught in the 1980s)when raised in the laboratory grew to the size of normal individuals (largerindividuals caught before 1980) The observed difference was attributed to adecreased growth rate due to the trawl fishery begun in the 1970s and theappearance of a new predator the Nile perch (Witte et al 1990) The decreasedbody depth of the dwarfed fish was hypothesised to be a result of increasedswimming activity because of predation pressure

The underlying hypothesis of this study based on the work of Meyer (1987) andWimberger (1991 1992) on New World cichlids was that feeding modes requiredfor ingestion of two diets would result in a morphological difference between thetwo groups through dynamic bone remodeling The purposes of this study were to(1) investigate feeding mode induced phenotypic plasticity of three species of mouthbrooders from Lake Malawi Labeotropheus fulleborni Ahl Melanochromis auratus(Boulenger) and M pyrsonotos (2) compare these results with the plasticityobserved in Old World substrate spawning Tilapia mariae Boulenger (spottedtilapia) and the New World substrate spawning cichlid Herichthys cyanoguttatum(Baird and Girard) (Rio Grande cichlid) and (3) test the hypothesis that observedmorphological trends were due to mode of feeding rather than dietary nutrition

MATERIALS AND METHODS

Wild-caught adults were bred in the laboratory and broods were collected andrandomly split in two feeding groups to block for genetic effects One group of eachbrood was fed brine shrimp naupli of Artemia species which requires a suctionmode of feeding whereas the second group was fed commercial flake food whichrequires a biting mode of feeding (Meyer 1987) Three broods of M pyrsonotos(69 individuals) three broods of M auratus (73 individuals) three broods of Lfuelleborni (64 individuals) one brood of H cyanoguttatum (66 individuals) andtwo broods of T mariae (50 individuals) were raised on these diets Temperaturephotoperiod substrate and aeration were kept constant among aquaria Aquariawere cleaned frequently to prevent grazing of algal growth

Following 5 months to 1 year of feeding (all young were raised until approxi-mately 50 mm however substrate spawning young which require a longer periodof time to reach a given size were usually raised for 9-12 months whereas mouthbrooding young were typically raised for 5-8 months) the broods were anaes-thetised and subsequently preserved in a 10 formalin solution After a week offormalin fixation the fish were placed in permanent storage in 70 ethanol A se-


ries of head and body truss measurements (Barel et al 1977) were made on eachindividual using dial calipers and JAVA image analysis software

Significant (P lt 005) differences of standard lengths between feeding modesof each brood were compared using ANOVA To investigate feeding mode-inducedphenotypic plasticity of three species of mouth brooders from Lake Malawi thefollowing head measurements were recorded for each brood head length lowerjaw length snout length postorbital head length horizontal eye diameter verticaleye diameter pre-orbital depth cheek depth and head depth Data were analysedusing sheared principal components analysis (SPCA) developed by Humphries etal (1981) Sheared principal components analysis restricts variation due to sizeto the first principal component so that the sheared second and third principalcomponents are strictly shape related Such an analysis which ordinates factorsindependently of a main linear ordination (Reyment et al 1984) permitted thedelineation of shape irrespective of size without having to rely on the use of ratios(Atchley 1978 Mosimann and James 1979 Humphries et al 1981 Reyment et al1984 Bookstein et al 1985) The covariance matrix was factored in the calculationof all sheared principal components

Each brood was analysed separately Differences among feeding groups for eachbrood of each species were illustrated by plotting the sheared second principalcomponent (SPCII) against the sheared third principal component (SPCIII) If theseclusters overlapped a MANOVA was used to determine if the clusters formed bythe minimum polygons of the sheared PCA scores for each treatment of each broodwere significantly different (P lt 005)

To compare the results observed in the Lake Malawi cichlids with substratespawning cichlids we collected and analysed data as described above using anOld World substrate-spawning cichlid T mariae Boulenger (spotted tilapia) andthe New World substrate-spawning cichlid H cyanoguttatum (Baird and Girard)(Rio Grande cichlid) In order to determine whether mouth-brooding restricts head-shape plasticity in cichlids we compared the average deviation (mm) among feedinggroups with significantly loaded head-shape characters

The hypothesis that head morphology changes were due to mode of feedingrather than nutrition was analysed in Metriaclima prysonotos using a flake fooddesigned specifically for this project by OSI Marine Lab Inc Burlingame CAUSA It was comprised of brine shrimp with a small amount of starch to hold theflake together without any added vitamins This flake therefore required a bitingmode of feeding but was nutritionally comparable to brine shrimp which requiresa suction mode of feeding The flakes did not differ in consistency or integrityOne brood of M pyrsonotos was randomly divided among two dietary treatments(1) commercial flake food or (2) OSI brine shrimp flake food and a second Mpyrsonotos brood was raised on (1) brine shrimp or (2) OSI brine shrimp flakefood Fish were maintained on their respective diets for a period of 6 months andshape analyses were conducted as above


RESULTS

Head morphology of Lake Malawi cichlids differed between feeding groups Whenthe SPCII was plotted against the SPCIII of the head morphometrics the minimumpolygon clusters that were formed for each of the two treatments (brine shrimp vscommercial flake food) in each of the three broods of each of the Lake Malawicichlids were significantly (P lt 005) different from each other (figs 1-3 broodswith the highest number for each species are pictured) The most heavily loadedcharacters were pre-orbital depth snout length lower-jaw length post-orbital headlength and cheek depth (tables 1-3) In eight of these nine broods lower jaw lengthwas one of the three variables that had the highest loadings in either SPCII orSPCIII When these variables were each plotted against standard length there wasno indication that any of the variables were impacted by allometric growth (egfig 4)

The minimum polygon clusters formed by plotting SPCAII versus SPCAIII forhead morphometrics of the two treatments of T mariae the Old World substrate-spawning species were not significantly different (P gt 005) for either of the twobroods (table 4 fig 5a b)

The minimum polygon clusters formed by plotting SPCAII versus SPCAIII of thetwo treatments for the head morphometrics of H cyanoguttatum the New Worldsubstrate-spawning species were significantly different (P lt 005 table 5 fig 6)

Four head-shape characters lower jaw length preorbital depth snout length andpost-orbital head length were highly loaded in H cyanoguttatum and Lake Malawimouth-brooding species A plot of the average deviation (mm) between feedinggroups for these four characters in L fuelleborni M auratus and M pyrsonotos the

Figure 1 Plot of sheared PCII versus PCIII of the head morphometric data of Labeotropheusfulleborni brood 1 fed brine shrimp and flake food


Figure 2 Plot of sheared PCII versus PCIII of the head morphometric data of Melanochromis auratusbrood 2 fed brine shrimp and flake food

Figure 3 Plot of sheared PCII versus PCIII of the head morphometric data of Metriaclima pyrsonotosbrood 2 fed brine shrimp and flake food

Old World mouth-brooding cichlids as compared to H cyanoguttatum indicatedthat mouth-brooding may inhibit phenotypic plasticity of head shape in Old Worldhaplochromine cichlids (fig 7) Although there were no observed differences inplasticity of lower jaw length deviation between dietary groups in preorbital depthsnout length and post-orbital head length was substantially less among mouth-brooding cichlids than in the H cyanoguttatum brood

For the M pyrsonotos brood in which one-half of the brood was fed commercialflake food and the other half brine shrimp flake food the minimum polygon clusters


Table 1Head morphometric measures and highest variable loadings of Labeotropheus fuelleborni broodsMeans and standard deviations for individuals fed brine shrimp are listed on the first line and thosefed flake food are on the second line Asterisks indicate significant differences (P lt 005) betweenfeeding groups and sample sizes are given in parentheses

Sheared PCII Mean Std Loading Sheared PCIII Mean Std LoadingCharacter Dev Character Dev

Percent head length Percent head lengthBrood 1 (14 23)

Lower jaw length 288 193 minus0742 Cheek depth 312 212 minus0794298 316 329 375

Preorbital depth 202 168 0473 Preorbital depth 202 168 0405224 142 224 142

Cheek depth 312 212 0395 Vertical eye diam 289 243 minus0313329 375 265 168

Brood 2 (2 3)Cheek depth 307 030 0870 Lower jaw length 294 088 minus0671

372 226 327 319Preorbital depth 210 311 minus0286 Horizontal eye 281 274 minus0546

258 226 diam 245 055Head length 320 093 0184 Preorbital depth 210 311 0307

316 142 258 226

Brood 3 (6 16)Preorbital depth 206 246 0816 Lower jaw length 291 184 minus0723

229 148 292 168Vertical eye diam 280 167 minus0358 Vertical eye diam 280 167 minus0417

255 138 255 138Lower jaw length 291 184 minus0293 Preorbital depth 206 246 minus0308

292 168 229 148

Figure 4 Plot of standard length (SL) versus lower jaw lengthSL of Labeotropheus fullebornibrood 1


Table 2Head and body morphometric measures and highest variable loadings of Melanochromis auratusbroods Means and standard deviations for individuals fed brine shrimp are listed on the first lineand those fed flake food are on the second line Asterisks indicate significant differences (P lt 005)between feeding groups and sample sizes are given in parentheses



Snout length 320 110 0569 Preorbital depth 197 100 minus0905317 189 177 100

Lower jaw length 280 083 minus0344 Cheek depth 682 173 0241290 148 701 106

Head depth 899 268 minus0322 Head depth 899 268 0200881 353 881 353

Brood 2 (14 20)Preorbital depth 173 178 minus0855 Horizontal eye 317 126 minus0567

190 166 diam 282 128Lower jaw length 286 107 0233 Snout length 282 180 0538

304 093 316 112Cheek depth 706 139 0214 Vertical eye diam 298 105 minus0426

694 212 269 118Brood 3 (9 8)

Horizontal eye 169 225 minus0655 Preorbital depth 280 177 0531diam 186 168 280 189

Preorbital depth 280 177 0481 Vertical eye diam 280 202 0510280 189 282 139


formed by plotting SPCAII versus SPCAIII for head morphometrics were notsignificantly (P gt 005) different (table 6 fig 8a)

For the M pyrsonotos brood in which one-half of the brood was fed live brineshrimp and the other half fed brine shrimp flake food the minimum polygonclusters formed by plotting SPCAII vs SPCAIII of the head morphometrics weresignificantly (P lt 005) different (table 7 fig 8b)

Size as indicated by standard length was different for many feeding modes (ta-ble 8) Herichthys cyanoguttatum and L fulleborni fed flake food were significantly(P lt 005) larger than those fed live brine shrimp as were two of three broodsof M auratus The third brood of M auratus was not significantly different be-tween feeding modes The part of one brood of M prysonotos fed live brine shrimpwas significantly larger than the siblings that were fed flake food there was nosignificant difference (P gt 005) in the feeding modes of the other two broodsThe portion of the brood of M prysonotos fed live brine shrimp was significantly


Table 3Head and body morphometric measures and highest variable loadings on Metriclima prysonotusMeans and standard deviations for individuals fed brine shrimp are listed on the first line and thosefed flake food are on the second line Asterisks indicate significant differences (P lt 005) betweenfeeding groups and sample sizes are given in parentheses



Postorbital head 526 692 minus0028 Preorbital depth 200 223 0570length 508 769 199 377

Snout length 266 234 minus0025 Snout length 266 234 0537254 437 254 437

Head length 338 129 minus0023 Postorbital head 526 692 minus0378341 189 length 508 769

Brood 2 (22 13)Preorbital depth 224 251 minus0791 Snout length 288 307 0687

215 291 262 263Snout length 288 307 0506 Vertical eye diam 255 267 minus0474

262 263 270 226Lower jaw length 270 296 0301 Preorbital depth 224 251 0309

250 333 215 291Brood 3 (5 5)

Preorbital depth 211 287 minus0878 Cheek depth 237 214 0644181 234 246 467

Lower jaw length 305 127 0274 Snout length 325 169 minus0624317 130 302 207

Horizontal eye 283 047 0236 Lower jaw length 305 127 0284diam 309 164 317 130

(P lt 005) larger than the portion fed brine shrimp flake food The portion of thebrood of M prysonotos fed commercial flake food was significantly (P lt 005)larger than that portion fed flake brine shrimp

DISCUSSION

In many cases there was no overlap between the clusters formed when the shearedsecond principal components were plotted against the sheared third principal com-ponents of the two feeding modes of certain broods (eg figs 1 2) Historically al-lopatric populations which exhibited such differentiation were regarded as separatespecies (Stauffer and McKaye 2001) Thus feeding mode induced phenotypic plas-ticity resulted in full siblings that were as different morphologically as sister speciesHanken (1983) demonstrated that relatively minor alterations in non-skeletal headregions of salamanders may effect a major change in overall head morphology The


Figure 5 Plot of sheared PCII versus PCIII of the head morphometric data of T mariae brood 1 (A)and brood 2 (B) fed brine shrimp and flake food

Figure 6 Plot of sheared PCII versus sheared PCIII of the head morphometric data of Hcyanoguttatum brood 1 fed brine shrimp and flake food

direction of the plasticity is similar to that found by Meyer (1987) with those indi-viduals fed brine shrimp having longer narrower heads than those fed flake foodIn particular lower-jaw length and preorbital depth were typically smaller and post-orbital head length and snout length typically larger in the brine-shrimp groups than


Table 4Head and body morphometric measures and highest variable loadings of Tilapia mariae broodsMeans and standard deviations for individuals fed brine shrimp are listed on the first line and thosefed flake food are on the second line Asterisks indicate significant differences (P lt 005) betweenfeeding groups and sample sizes are given in parentheses



Lower jaw length 261 141 minus0633 Preorbital depth 184 107 0540316 274 224 170

Horizontal eye diam 384 196 0502 Horizontal eye diam 384 196 minus0525315 368 315 368

Vertical eye diam 357 196 0354 Postorbital head 386 185 0464308 226 length 389 124

Brood 2 (29 12)Lower jaw length 236 188 minus0896 Preorbital depth 195 171 minus0838

264 289 223 153Postorbital head 385 237 0224 Postorbital head 385 237 0357

length 384 118 length 384 118Preorbital depth 195 171 0220 Cheek depth 318 206 0344

223 153 317 177

Table 5Head and body morphometric measures and highest variable loadings of Herichthys cyanoguttatumbroods Means and standard deviations for individuals fed brine shrimp are listed on the first lineand those fed flake food are on the second line Asterisks indicate significant differences (P lt 005)between feeding groups and sample sizes are given in parentheses



Preorbital depth 172 206 minus0740 Postorbital head 445 234 minus0725217 335 length 421 305

Postorbital head 445 234 0373 Snout length 288 209 0359length 421 305 338 332

Lower jaw length 273 119 0342 Preorbital depth 172 206 minus0320286 208 217 335

the flake-food groups The hypothesis that changes in head morphology are due tothe mode of feeding rather than dietary nutrition was supported by the results of thefeeding experiments using the brine shrimp flake food The head morphology of theM pyrsonotos brood fed brine shrimp flakes and commercial flakes was not signif-


Figure 7 Plot of the mean deviation (mm) between feeding groups for four head-shape charactersin Labeotropheus fulleborni Melanochromis auratus Metriaclima pyrsonotos and Hererichthyscyanoguttatum (LJL = lower jaw length PRED = pre-orbital depth SNL = snout length and POHL= postorbital head length)

Table 6Head and body morphometric measures and highest variable loadings of Metriaclima pyrsonotosMeans and standard deviations for individuals fed brine shrimp flake food are listed on the first lineand those fed commercial flake food are on the second line Asterisks indicate significant differences(P lt 005) between feeding groups and sample sizes are given in parentheses



Preorbital depth 227 300 minus0804 Vertical eye diam 325 169 0738208 260 302 207

Snout length 348 427 0397 Horizontal eye diam 276 161 0483287 276 289 240

Postorbital head 406 072 0253 Lower jaw length 324 162 minus0403length 399 188 328 247

icantly different (P gt 005 same feeding mode) whereas significant (P lt 005)differences existed between the brood fed brine shrimp and brine shrimp flakes (dif-ferent feeding modes)

Moreover one could argue that the changes reported herein could be a result ofchanges in scale which result in allometric growth (Strauss 1984) Certainly otherfishes such as dwarf Coregonus species exhibit changes in body shape which maybe related to differences in size (Shields and Underhill 1993) as well as changes inspawning times and life span (Swardson 1949 1950 Fenderson 1964 Lindsey etal 1970 Smith and Todd 1984) Although we observed differences in size between


Table 7Head and body morphometric measures and highest variable loadings of Metriaclima pyrsonotosMeans and standard deviations for individuals fed brine shrimp are listed on the first line and those fedbrine shrimp flake food are on the second line Asterisks indicate significant differences (P lt 005)between feeding groups and sample sizes are given in parentheses



Preorbital depth 240 199 minus0624 Snout length 328 150 0654203 210 316 270

Horizontal eye diam 268 295 minus0479 Cheek depth 340 197 minus0518276 226 357 236

Snout length 328 150 0370 Lower jaw length 333 191 minus0340316 270 353 228

Table 8Comparisons of standard lengths (mm) between feeding broods

Species Live brine shrimp Commercial flake food Flake brine shrimp

Herichthys cyanoguttatum 292 480Labeotropheus fulleborni 414 610Labeotropheos fulleborni 600 834Labeotropheos fulleborni 410 643Melanochromis auratus 159 157Melanochromis auratus 341 401Melanochromis auratus 426 473Metriaclima prysonotos 316 254Metriaclima prysonotos 363 357Metriaclima prysonotos 396 336Metriaclima prysonotos 597 444Metriaclima prysonotos 558 480Tilapia mariae 472 897Tilapia mariae 391 567

Indicates significant differences between feeding modes (P lt 005)

feeding modes within broods the fact that there was no relationship between anyof the head morphometrics and standard length (eg fig 4) refutes this hypothesisMoreover significant differences in standard length were observed for both broodsof T marie however no differences in shape of individuals exposed to differentfeeding modes was observed for this species

The magnitude of head shape plasticity observed in the New World substrate-spawning cichlid H cyanoguttatum was greater than that observed in the OldWorld haplochromine cichlids Thus these data suggest that mouth brooding mayconstrain the plasticity of jaw morphology in the latter however the comparison


Figure 8 Plot of sheared PCII versus PCIII of the head morphometric data of Metriaclima pyrsonotosfed commercial flake food and brine-shrimp flake food (A) and brine shrimp and brine-shrimp flakefood (B)

with T mariae may indicate that New World cichlids simply exhibit more plasticitythan do Old World cichlids Similar experiments should be conducted on LakeTanganyika mouth brooders vs substrate spawners

Implications for alpha-level taxonomy

Because of the current lack of detectable fixed genetic differentiation among closelyrelated Lake Malawi cichlids (McKaye et al 1982 Moran and Kornfield 1993Stauffer et al 1993) most haplochromine cichlids are described on the basis ofmorphology alone For example characteristics of the pharyngeal bone and jawmorphology have often played an important part in species descriptions of OldWorld cichlids (Greenwood 1981) Stauffer and Boltz (1989) described a newspecies of Metriaclima from Lake Malawi and found that the characters differen-tiating it from congeners (cheek depth post-orbital head length pre-orbital depthand size of the dentigerous area of the pharyngeal bone) were ones that could beinfluenced by feeding mode (Kornfield et al 1982 Meyer 1987 Wimberger 19911992 Stauffer et al 1995) Similar results were found in the genus Petrotilapia


(Marsh 1983 Stauffer and van Snik 1996) Conversely Sturmbauer and Meyer(1993) note that heterospecific populations are particularly prone to homoplasy withrespect to character states associated with foraging Therefore it is necessary tostudy the ecology behavior genetics and breeding coloration of these species in or-der to substantiate their specific status as suggested by morphological data (Staufferand McKaye 1986 Stauffer and Boltz 1989)

Implications for rapid radiation of haplochromine cichlids

Wimberger (1991) considered phenotypic plasticity an evolutionary factor that re-sults in morphological diversification Vertebrate resource polymorphisms may sig-nificantly contribute to population divergence and speciation (Smith and Skulason1996) Skulason and Smith (1995) suggest that resource polymorphisms are impor-tant entities in the initial phases of speciation and Day et al (1994) concluded thatphenotypic plasticity is evolutionarily labile Rice and Hostert (1993) further sug-gest that if traits important in resource use are associated with those important inisolation then reproductive isolation can occur via genetic hitchhiking Certainlydifferences in mouth shape eye size (Lindsey 1981) gill-raker morphology (Mag-nuson and Heitz 1971 Chapman et al 2000) and pharyngeal-mill morphology(Liem 1974 1979) can all contribute to feeding diversification which in turn canlead to habitat preferences and isolation of selected morphs In his discussion of eco-logical speciation Schluter (1996) suggests that mating preferences may diverge ifthe selection criteria are associated genetically with phenotypic traits Differencesin phenotypes can be as dramatic as those found in four sympatric morphs of thearctic char Salvelinus alpinnus (Hindar 1994) trophic morphs of the tiger sala-mander Ambystoma tigrinum (Collins 1981) and larval morphs of the spadefoottoad Scaphiopus spp (Pomeroy 1981) Morphological plasticity however mustbe linked with parameters that promote genetic isolation (eg behavioural barriershabitat isolation) in order for it to influence speciation rates (Lovell 1989) Robin-son and Wilson (1994) provide such evidence by stating that genetic differentiationis linked to phenotypic differences in 19 of 48 lacustrine fish species MoreoverMcPhail (1984 1994) and Lavin and McPhail (1987) have demonstrated that phe-notypic differences between benthic and pelagic forms of sticklebacks persist whendifferent morphs are cultured in the laboratory and provided with the same diet

The driving mechanism for the speciation events which led to the explosive radia-tion of the haplochromine cichlids in the Great Lakes of Africa is undiscovered thetwo most widely proposed methods are allopatric speciation accelerated by fluctu-ation in lake levels (Fryer 1959 Marlier 1959 Fryer and Iles 1972 Greenwood1974 1981 1982 McKaye and Gray 1984) and intrinsic isolating mechanisms suchas assortative mating (Kosswig 1947 1963 Bush 1975 McKaye 1978 1980McKaye and Stauffer 1986 Stauffer et al 2002) Irrespective of the mechanismprimarily responsible for the high diversity the relationship between phenotypicmorphs and speciation is currently unknown Unquestionably a colonising speciespossessing a high degree of phenotypic plasticity may have a selective advantage be-


cause of the ability to exploit different resources in differing environments (Lewon-tin 1965) and phenotypic plasticity may be an important factor which allows somany species to coexist in the African lakes A necessary first step in assessing therelationship if any between polymorphism and speciation is to determine the ex-tent that environmental influences have on the morphology of natural populationsFor example one New World cichlid H minckleyi has achieved trophic radiationthrough polymorphism (Sage and Selander 1975 Kornfield et al 1982) A strongpharyngeal bone with molariform teeth was found in the form feeding on snailswhereas a less developed pharyngeal bone with villiform teeth was found in theform feeding on softer food items (Kornfield et al 1982) In this case the environ-ment was not only the broker of selection but was also the agent of developmentthat directed the range of phenotypes that were created (West-Eberhard 1989)

The observed plasticity in the rock-dwelling Malawi cichlids may have facilitatedtheir extensive trophic radiation and subsequent explosive speciation Lake Malawiis the most speciose lake in the world with regard to fishes (Kocher et al 1993) Cer-tainly variation which supplies the raw material for evolutionary change originateswith both the genotype and the phenotype (Stearns 1989) While some argue thatphenotypic plasticity retards evolution (Wright 1931) Dobshansky (1951) theo-rised that phenotypic modulation provided the necessary changes during evolutionPlasticity can be considered as an evolutionary factor that results in morphologi-cal diversification (Wimberger 1991) If the environmental stimulus directing theplasticity is fluctuating selection for maintenance of plasticity may occur If theenvironmental stimulus is constant and directional however genetic assimilationof the new phenotype could occur over time (Waddington 1975 Chapman et al2000) Trophic polymorphism has been proposed as an intermediate step towardsspeciation (Sage and Selander 1975) Polymorphism and genetic assimilation ofplastic traits may be a speciation mechanism in Old World haplochromine cich-lids Although additional studies of the phenotypic plasticity of Old World Tilapiaspecies are needed the absence of explosive radiation as observed in Malawi hap-lochromine species in the substrate spawning Tilapia species may be related to thereduced level of plasticity observed in T mariae

Alternatively other authors (Wimberger 1994) have suggested that althoughphenotypic plasticity itself does not contribute to speciation if coupled with factorspromoting reproductive isolation of morphs such as assortative mating speciationmay result Sexual selection has been suggested as a factor in the acceleratedspeciation of many of the Lake Malawi cichlids (Dominey 1984 McKaye 1991)and if sexual selection for particular trophic morphs occurs speciation can beaccelerated (Dominey 1984 OrsquoDonald and Majerus 1985) If Wimberger (1994)is correct phenotypic plasticity may have provided the raw material on whichassortative mating cued

Many authors have postulated that behavioural characteristics are frequently theinitial part of the phenotype which evolves (Mayr 1963 1974 Corning 1974Wyles et al 1983 Weislo 1989) West-Eberhard (1989) summarised several


reasons why plastic traits may initiate new directions in the evolution of a speciesand concluded that labile plastic traits such as behaviour are more likely to result ina favorable variant Stauffer et al (1995) postulated that colour forms of many of theLake Malawi rock-dwelling cichlids as well as the bowers (spawning platforms) ofthe sand-dwelling cichlids are manifestations of behavioural characteristics and canbe used to delimit sibling species such circumstantial evidence supports the theorythat phenotypic plasticity aided in the rapid radiation of the Old World cichlids

ACKNOWLEDGEMENTS

We are indebted to MS Lamon and OSI Marine Lab Inc for designingmanufacturing and supplying us with the brine shrimp flake food Many studentsassisted with fish care including KL Bryan I Posner ET Hennenhoefer KAKellogg DJ Parise RA Ruffing TD Stecko J Stingelin T Stowe K Walterand Z Whisel The authors benefited from discussions with T Levitt-Gilmour Thisstudy was partially supported with a University Scholars Research Grant PennState

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Fryer G (1959) The trophic interrelationships and ecology of some littoral communities of LakeNyasa with special reference to the fishes and a discussion of the evolution of a group of rock-frequenting Cichlidae Proc Zool Soc London 132 153-282

Fryer G amp Iles TD (1972) The Cichlid Fishes of the Great Lakes of Africa Their Biology andEvolution Oliver and Boyd London

Greenwood PH (1965) Environmental effects on the pharyngeal mill of a cichlid fish Astatore-ochromis alluadi and their taxonomic implications Proc Linnean Society of London 176 1-10

Greenwood PH (1974) The cichlid fishes of Lake Victoria East Africa The biology and evolutionof a species flock Bulletin of the British Museum of Natural History Supplement 6 1-34

Greenwood PH (1981) East African Cichlid Fishes The Haplochromine Fishes of the East AfricanLakes Bulletin of the British Museum of Natural London

Greenwood PH (1982) The haplochromine fishes of the east African lakes Kraus InternationalPublications Munchen and British Museum Natural History London

Hanken J (1983) Miniaturization and its effects on cranial morphology in plethodontid salamandersgenus Thorius (Amphibia Plethodontidae) II The fate of the brain and sense organs and their rolein skull morphogenesis and evolution J Morphol 177 255-268

Hindar K (1994) Alternative life histories and genetic conservation In V Loeschke J Tomink ampSK Jain (Eds) Covservation Genetics pp 323-336 Birkhauser Basel

Hinton RJ amp McNamara JA Jr (1984) Effect of age on the adaptive response of the adulttemporomandibular joint Ang Orthod 54 154-162

Hoogerhoud RJC (1984) A taxonomic reconsideration of the Haplochrime genera GaurochromisGreenwood 1980 and Labrochromis Regan 1920 (Pisces Cichlidae) Neth J Zool 34 539-565

Humphries JM Bookstein FL Chernoff R Smith GR Elder RL amp Poss SG (1981)Multivariate discrimination by shape in relation to size Systematic Zoology 30 291-308

Huysseune A Sire J-Y amp Meunier FJ (1994 Comparative study of lower pharyngeal jaw structurein two phenotypes of Astatereochromis alluaudi (teleostei Cichlidae) J Morphol 221 2543

James FC (1983) Environmental component of morphological variation in birds Science 221 184-186

Kocher TD Conroy JA McKaye KR amp Stauffer JR Jr (1993) Similar morphologies ofcichlid fish in lakes Tanganyika and Malawi are due to convergence Molecular Phylogeneticsand Evolution 2 158-165

Kornfield ID Smith C Gagnon PS amp Taylor JN (1982) The cichlid fish of Cuatro CiengasMexico Direct evidence of conspecifity among distinct trophic morphs Evolution 36 658-664

Kornfield I amp Taylor JN (1983) A new species of polymorphic fish Cichlasoma minckleyi fromCuatro Ciengas Mexico (Teleostei Cichlidae) Proc Biol Soc Washington 96 253-269

Kosswig C (1947) Selective mating as a factor for speciation in cichlid fish of east African lakesNature 159 604-605

Kosswig C (1963) Ways of speciation in fishes Copeia 1963 238-244


Lavin PA amp McPhail JD (1987) Morphological divergence and the organization of trophiccharacters among lacustrine populations of the threespine stickleback (Gasterosteus aculeatus)Canadian Journal of Fisheries and Aquatic Sciences 44 1820-1829

Legler JM (1981) The taxonomy distribution and ecology of the Australian freshwater turtles(Testudines Pleurodira Chelidae) Nat Geog Soc Res Rept 13 391-404

Levins R (1968) Evolution in changing environments Princeton University Press Princeton USALewontin RC (1965) Selection for colonizing ability In HG Baker amp GL Stebbins (Eds) The

Genetics of Colonizing Species pp 77-94 Academic Press New York USALiem KF (1974) Evolutionary strategies and morphological innovations cichlid pharyngeal jaws

Systematic Zoology 20 425-441Liem KF (1979) Modulatory multiplicity in the feeding mechanism in cichlid fishes as exemplified

by the invertebrate pickers of Lake Tanganyika J Zool London 189 93-125Lindsey CC (1981) Stocks are chameleons plasticity in gill rakers of coregonid fishes Canadian

Journal of Fisheries and Aquatic Sciences 38 1497-1506Lindsey CC Clayton JW amp Franzion WG (1970) Zoogeographic problems and protein variation

in the Coregonus clupeaformis whitefish species complex In CC Lindsey amp CS Woods (Eds)Biology of Coregonine Fishes pp 127-146 University of Manitoba Press Winnipeg USA

Lovell T (1989) Nutrition and feeding of fish Van Nostrand Reinhold New York USAMagnuson JJ amp Heitz JG (1971) Gill raker apparatus and food selectivity among mackerels tunas

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citrinellum and its relevance to sympatric speciation in the family Cichlidae EnvironmentalBiology of Fishes 5 75-78

McKaye KR (1991) Sexual selection and the evolution of the cichlid fishes of Lake MalawiAfrica In MHA Kenleyside (Ed) Cichlid fishes Behavior ecology and evolution pp 241-257Chapman amp Hall London

McKaye KR amp Gray WN (1984) Extrinsic barriers to gene flow macrohabitat heterogeneity ofLake Malawi and reef colonization patterns of rock-dwelling cihclids In A Echelle amp I Kornfield(Eds) Evolution of Species Flocks pp 169-184 University of Maine Press USA

McKaye KR Kocher TD Reinthal P amp Kornfield I (1982) Genetic analyses of a sympatricspecies complex of Petrotilapia Trewavas (Teleostei Cichlidae) J Linnean Soc 76 91-96

McKaye KR amp Stauffer JR Jr (1986) Description of a gold cichlid Pseudotropheus barlowi(Teleostei Cichlidae) from Lake Malawi Africa Copeia 1986 870-875

McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus) morphologicaland genetic evidence for a species pair in Enos Lake British Columbia Canadian Journal ofZoology 62 1402-1408

McPhail JD (1994) Speciation and the evolution of reproductive isolation in the sticklebacks(Gasterosteus) of southwestern British Columbia In MA Bell amp SA Foster (Eds) Evolution ofthe Threespine Stickleback pp 399-437 Oxford University Press Oxford

Meyer A (1987) Phenotypic plasticity and heterochrony in Cichlasoma managuense (PiscesCichlidae) and their implications for speciation in cichlid fishes Evolution 41 1357-1369

Meyer A (1990) Ecological and evolutionary consequences of the trophc polymorphism in Cichla-soma citrinellum (Pisces Cichlidae) Biological J Linnean Soc 39 279-299


Moran P amp Kornfield I (1993) Retention of an ancestral polymorphism in the mbuna species flock(Pisces Cichlidae) of Lake Malawi Molecular Biology and Evolution 10 1015-1029

Mosimann JE amp James FC (1979) New statistical methods for allometry with application to Floridared-winged blackbirds Evolution 33 444-459

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OrsquoDonald P amp Majerus MEN (1985) Sexual selection and the evolution of preferential mating inladybirds I Selection for high and low lines of female preference Heredity London 55 401-412

Page LM amp Burr BM (1991) A Field Guide to Freshwater Fishes Houghton Mifflin CompanyBoston

Pomeroy LV (1981) The ecological and genetic basis of polymorphism in the larvae of spadefoottoads Scaphiopus Unpublished PhD thesis Univ Calif Riverside

Reyment RA Blackith RE amp Cambell NA (1984) Multivariate mrophometrics (2nd ed)Academic Press New York

Rice WR amp Hostert EE (1993) Laboragory experiments on speciation mdash what have we learned in40 years Evolution 47 1637-1653

Robinson BW amp Wilson DS (1994) Character release and displacement in fishes a neglectedliterature American Naturalist 144 596-627

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Schlichting CD (1986) The evolution of phenotypic plasticity in plants Annual Review of Ecologyand Systematics 17 667-693

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Schluter D (1996) Ecological speciation in postglacial fishes Philosophical Transactions of theRoyal Society of London B 351 807-814

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Skulason S amp Smith TB (1995) Resource polymorphisms in vertebrates Trends Ecol Evol 10366-370

Smith GR amp Todd TN (1984) Evolution of species flocks of fishes in north temperate lakes InAA Eschelle amp I Kornfield (Eds) Evolution of Fish Species Flocks pp 45-68 University ofMaine at Orono Press Orono

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Smith-Gill SJ (1983) Developmental plasticity Developmental conversion versus phenotypicmodulation American Zoologist 23 47-55

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Stauffer JR Jr LoVullo TJ amp McKaye KR (1993) Three new sand-dwelling cichlids from LakeMalawi Africa with a discussion of the status of the genus Copidachromis (Teleostei Cichlidae)Copeia 1993 1017-1027


Stauffer JR Jr amp McKaye KR (1986) Description of a paedophagous deep-water cichlid(Teleostei Cichlidae) from Lake Malawi Africa Proc Biol Soc Washington 99 29-33

Stauffer JR Jr amp McKaye KR 2001 The naming of cichlids Cichlid Research State of the ArtJournal of Aquariculture and Aquatic Sciences 9 1-16

Stauffer JR Jr McKaye KR amp Konings AF (2002) Behaviour an important diagnostic tool forLake Malawi cichlids Fish and Fisheries 2002 213-224

Stauffer JR Jr amp van Snik ES (1996) New species of Petrotilapia (Teleostei Cichlidae) fromLake Malawi Africa Copeia 3 695-702

Stearns SC (1989) The evolutionary significance of phenotypic plasticity BioScience 39 436-445Strauss RE 1984 Allometry and functional feeding morphology in haplochromine cichlids In AA

Eschelle amp I Kornfield (Eds) Evolution of Fish Species Flocks pp 217-229 University of MaineOrono

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Waddington CH (1975) The evolution of an evolutionist Cornell University Press Ithaca New YorkWest-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity Annual Review of

Ecology and Systematics 20 249-278Weislo WT (1989) Behavior as a pacemaker of evolution Annual Review of Ecology and Systemat-

ics 20 137-169Williams CK amp Moore RJ (1989) Phenotypic adaptation and natural selection in the wild rabbit

Oryctolagus cuniculus in Australia J Anim Ecol 58 495-508Wimberger PH (1991) Plasticity of jaw and skull morphology in the neotropical cichlids Geophagus

brasiliensis and G steindachneri Evolution 45 1545-1563Wimberger PH (1992) Plasticity of fish body shape The effects of diet development family and age

in two species of Geophagus (Pisces Cichlidae) Biol J Linnean Soc 45 197-218Wimberger PH (1994) Trophic polymorphisms plasticity and speciation in vertebrates In DJ

Stouder amp K Fresh (Eds) Advances in Fish Foraging Theory and Ecology Belle Baruch PressColumbia South Carolina

Witte F (1984) Consistency and functional significance of morphological differences between wildcaught and domestic Haplochromis squamipinnis (Pisces Cichlidae) Neth J Zool 34 596-612

Witte F Barel CDN amp Hoogerhoud RJC (1990) Phenotypic plasticity of anatomical structuresand its ecomorphological significance Neth J Zool 40 278-298

Woltereck R (1909) Weitere experimentelle Untersuchungen uber Artveranderung speziell uber dasWesen quantitativer Artunterschiede bei Daphniden Verhandlungen der Deutschen ZoologischenGesellschaft 1909 110-172

Wright S (1931) Evolution in mendelian populations Genetics 16 97-159Wyles JS Kunkel JG amp Wilson AC (1983) Birds behavior and anatomical evolution Proc Nat

Acad Sciences USA 80 4394-4397


reptiles (Legler 1981) birds (James 1983) mammals (Williams and Moore1989) insects (Atchley 1971) and plants (Bradshaw 1965 Schlichting 1986)Two types of phenotypic plasticity developmental conversion and phenotypicmodulation can be characterised by direction and magnitude respectively (Smith-Gill 1983) Developmental conversion results in discrete morphs in response to anenvironmental cue (Stearns 1989 West-Eberhard 1989) Levins (1968) postulatedthat such conversions can be controlled by developmental switches or controllersthat determine attributes For example gender in turtles is determined by incubationtemperature Such switches can be non-plastic and under strict allelic control (Mayr1963) In contrast phenotypic modulations or reaction norms result in continuousvariation of a particular trait in response to an environmental stimulus (Woltereck1909 Stearns 1989) The direction and magnitude of phenotypic modulation maybe similar or different for related species (Schlichting 1986) The plasticity of thetrait itself is affected by natural selection and as such is under genetic control(Bradshaw 1965 West-Eberhard 1989) thus a given reaction norm may havea distinct evolutionary trajectory different from the plasticity with which it isassociated (Schlichting and Levin 1986)

The Great Lakes of Africa including lakes Malawi Tanganyika and Victoriaharbour the most speciose ichthyofauna of any of the worldrsquos lakes (Fryer and Iles1972 Kocher et al 1993) The endemic haplochromine cichlid fishes provide oneof the best examples of explosive vertebrate speciation Despite the morphologicalplasticity which has been observed in other fishes due to such environmental factorsas diet (Meyer 1987) temperature (Stearns 1989 Page and Burr 1991) light(Witte et al 1990) and predation pressure (Witte et al 1990) some authors haveassumed the morphology of African cichlid fishes to be developmentally canalised(van Oijen 1982)

Observed morphological variability observed in the Cichlidae may be due in partto phenotypic plasticity (Hoogerhoud 1984 Meyer 1987 1990a 1990b Witte et al1990 Wimberger 1991 1992) Witte (1984) hypothesised that differences in pre-maxilla development in wild-caught vs aquarium-raised Haplochromis squamipin-nis Regan from Lake George were due to differences in diet Hoogerhoud (1984)noted diet-dependent differences in the pharyngeal jaw apparatus of Gaurochromisand Labrochromis to be of the same magnitude as differences between these twogenera Furthermore the phenotypic divergence of the pharyngeal apparatus of theNew World Herichthys minckleyi (Kornfield and Taylor 1983) exceeds that ob-served among species of molluscivorous cichlids inhabiting Lake Victoria (Hooger-houd 1984) Differences in bone structure of the lower pharyngeal jaw associatedwith Astateroeochromis alluadi Pellegrin that were fed different diets were noted(Huysseune et al 1994 Smits et al 1996a b)

Meyer (1987) and Winberger 1991 1992) have directly tested the effects ofdiet on phenotypic plasticity in New World cichlids In general cichlid speciesthat feed by biting tend to have a short blunt (obtusorostral) snout whereasspecies that rely heavily on suction have a long pointed (acutorostral) snout (Barel


















RESULTS





















316 142 258 226




292 168 229 148












694 212 269 118Brood 3 (9 8)

















250 333 215 291Brood 3 (5 5)





DISCUSSION
















223 153 317 177
















































ACKNOWLEDGEMENTS


REFERENCES



























































































































RESULTS





















316 142 258 226




292 168 229 148












694 212 269 118Brood 3 (9 8)

















250 333 215 291Brood 3 (5 5)





DISCUSSION
















223 153 317 177
















































ACKNOWLEDGEMENTS


REFERENCES

























































































































316 142 258 226




292 168 229 148












694 212 269 118Brood 3 (9 8)

















250 333 215 291Brood 3 (5 5)





DISCUSSION
















223 153 317 177
















































ACKNOWLEDGEMENTS


REFERENCES




















































































































694 212 269 118Brood 3 (9 8)

















250 333 215 291Brood 3 (5 5)





DISCUSSION
















223 153 317 177
















































ACKNOWLEDGEMENTS


REFERENCES




















































































































250 333 215 291Brood 3 (5 5)





DISCUSSION
















223 153 317 177
















































ACKNOWLEDGEMENTS


REFERENCES
























































































































223 153 317 177
















































ACKNOWLEDGEMENTS


REFERENCES


















































































































































ACKNOWLEDGEMENTS


REFERENCES










































































































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