Traditionally, reproductive isolation between disjoint populations has been thought to emerge as a result of the accumulation of different mutations, genetic drift, or through the effects of natural and sexual selection^1^. Alternatively, the ability of an organism to express different phenotypes depending on the environment (i.e. phenotypic plasticity) could produce reproductive isolation^2,3^. Sexually selected traits are expected to be phenotypically plastic and can result in modifications of the species recognition system and thus originate new species^4^. Here we show that the population-characteristic male courtship behaviour of a fish (Girardinichthys multiradiatus) is modified in the presence of females from other populations, that this is due to the males responding to subtle cues from females, and that they fail to emulate the female&#x27;s population-characteristic behaviour. We conclude that plasticity has led to the creation of local dialects in the courtship pattern that hampers communication between heterogametic individuals and promotes pre-mating isolation

Adriana Vallarino

Cesar Gonzalez Zuarth

Constantino Macias Garcia

English

Nature Precedings

1 
Courtship plasticity reveals the evolution of dialects in 
allopatric fish populations 
Cesar Gonzalez-Zuarth, Adriana Vallarino and Constantino Macias Garcia 
Instituto de Ecología, Universidad Nacional Autónoma de México. A.P. 70-275. México 
D.F. 04510. ‘These authors contributed equally to this work’ 
 
Traditionally, reproductive isolation between disjoint populations has been 
thought to emerge as a result of the accumulation of different mutations, genetic 
drift, or through the effects of natural and sexual selection1. Alternatively, the 
ability of an organism to express different phenotypes depending on the 
environment  (i.e. phenotypic plasticity) could produce reproductive isolation2, 3. 
Sexually selected traits are expected to be phenotypically plastic and can result in  
modifications of the species recognition system and thus originate new species4. 
Here we show that the population-characteristic male courtship behaviour of a fish 
(Girardinichthys multiradiatus) is modified in the presence of females from other 
populations, that this is due to the males responding to subtle cues from females, 
and that they fail to emulate the female's population-characteristic behaviour. We 
conclude that plasticity has led to the creation of local dialects in the courtship 
pattern that hampers communication between heterogametic individuals and 
promotes pre-mating isolation.  
Phenotypic plasticity evolves to maximize fitness in variable environments5, 6. It has 
been proposed that behaviour is an especial aspect of the phenotype and can initiate new 
directions of evolutionary change because it is labile and can be modified abruptly 
without the necessity of genetic change2, 3. In isolation, mate choice patterns in 
populations can evolve independently from each other as a result of random or adaptive 
2 
differences in the trajectory of males’ traits7and females preferences. As a consequence, 
the pattern of courtship of males becomes a sign of local identity8. Thus the pattern of 
courtship can be used by females as a signal indicating that males are adapted to a 
particular environment, and females can increase their fitness by choosing local males 
to mate with9. Because a mistake in the identification of the males' courtship can imply 
an increase in the cost of reproduction, females are being pressed by sexual selection to 
mate with the appropriate males. Through frequency-dependent selection, 
developmental plasticity may generate divergence and contribute to the evolution of 
reproductive isolation. Male courtship behaviour evolves to capture female attention, 
thus attracting potential partners and facilitating mating. Courtship can vary between 
populations within the bounds permitted by the environment10, 11. This variation can be 
the result of 1) selection acting on congenital variants, or 2) phenotypic plasticity, like 
song or display learning12. 
Girardinichthys multiradiatus is a viviparous fish from Central México with an 
elaborated courtship pattern and effective female mate choice 8,13. In a previous work 
we found that males of this species showed geographic variation on sexual behaviour8, 
therefore, here we evaluated whether this variation was a consequence of 
communication failure between heterogametic individuals during courtship. As a 
preliminary step we re-analysed data published elsewhere8 and determined that the 
tendency to perform different elements of the courtship sequence varies predictably 
between males from five populations. Moreover, the male courtship sequences are 
associated with their population of origin with substantially greater accuracy than 
expected by chance (Table 1), suggesting that males of all populations have developed a 
particular pattern of courtship. We then evaluated whether female choice was 
responsible for this geographical variation. We recorded female behaviour during 
courtship, and found that females respond differently to the courtship from 
heterogametic males than that from their own males (Table 2). Finally we compared the 
3 
courtship style of males when encountering females from their own populations with the 
courtship they display when facing females from other populations in order to 
investigate whether males' courtship sequence was influenced by the behaviour of the 
females to which it was directed13-15. We found that males’ courtship to females from 
their population significantly differed from the courtship showed to heterogametic 
females (Table 3). These results indicate that males are capable of recognizing 
homogametic from heterogametic females and adjust their courtship depending on each 
females' behaviour. 
We suggest that when males court allopatric females they evoke unfamiliar 
patterns of female responses, causing males to modify their courtship style. This 
behavioural modification demonstrates that courtship in the Amarillo fish is plastic, 
even if the adjustment is insufficient to establish appropriate communication with 
heterogametic females. Such signal mismatch is characteristic of bird song dialects, 
whose origin is unknown17. In the Amarillo fish local variation in courtship style may 
be ultimately due to different environmental constraints such as water turbidity or type 
of predators18, but may arise through behavioural plasticity which enables fish to adjust 
their courtship patterns and become more efficient in their particular environment, 
giving rise to population-specific courtship styles. 
If males are plastic in their courtship behaviour, why then were they unable to 
adjust their behaviour (using the females' feedback) so as to emulate the courtship style 
of the female's population? The reason is unlikely to be simply the cost of plasticity 19,20 
as they did modify their courtship style. What seems to be the case is that both male 
courtship style and female responses to this have co-diverged within populations, so that 
males encountering unexpected female reactions adjusted their behaviour as they would 
have done if a homogametic female had changed her behaviour,. Our data are thus 
compatible with the idea that populations of the Amarillo fish have courtship dialects 
4 
evidenced by differences in 1) male courtship style, 2) female reactions to male 
courtship elements, and 3) male reactions to female behavioural feedback. These 
findings support the idea that phenotypic plasticity is capable of originating 
reproductive isolation between allopatric populations. 
Methods 
We collected 270 males and 270 females from 5 allopatric populations along the range 
of distribution of this species11. Fish were taken to the laboratory and placed in 40 l 
tanks where they were fed with commercial flakes twice a day and were exposed to a 
12h light photoperiod. After 15 days fish were separated by sexes and they were placed 
into individual plastic containers. This procedure not only allowed us to identify the fish 
individually but as previous work had shown, let us also increase the motivation of the 
fish to court. 
In order to study the geographical variation in the courtship of males, we 
compared the pattern of displays used by males when courting homogametic and 
heterogametic females registering frequency and time that males executed behaviours 
associated with intense courtship (i.e. dynamic display behaviours: fin folding, flagging, 
and figure of eight), behaviours associated with fins' exhibition (static display 
behaviours: lateral fin display and frontal fins display) and copulation attempts12. This 
procedure was repeated with each combination of populations and each fish was used 
only in one trial. In order to know the variation in females’ responses, the sequence of 
displays of males during courtship and the correspondent female responses (vibration, 
escape, biting, approach to the male, swimming together with the male, no response to 
the displays), were filmed for 15 minutes. Five homogametic females and five 
heterogametic females from each population were filmed. 
5 
Discriminant analysis. We verified that courtship style is population-specific by 
performing a canonical discriminant analysis of courtship sequences performed by 
males to females from their own population and the results were cross validated using 
the software S-Plus v.2 (MathSoft Inc.). We used population as grouping variable and 
behavioural displays during courtship as independent variables. 
Cochran's Q test. We used Cochran Q test, an extension of McNemar's test for for the 
significance of changes, that can be used when k (samples) > 2) to analyze female 
responses to dynamic display behaviours (fin folding, flagging, figure of eight and 
copulation attempts), and to postural fin displays (lateral display and frontal display)  
Responses were quantified as 1 (if a given heterogametic female did performed one of 
the responses shown by homogametic females faced with the same courtship behaviour) 
or  0 (when the behaviour evoked by the male display was different to that shown by 
heterogametic females). 
1. Coyne, J. A. & Orr, H. A. The evolutionary genetics of speciation. Phil Trans. 
Roy. Soc. Lond. B 353, 287-305 (1998). 
2. West-Eberhard, M. J. Developmental plasticity and the origin of species 
differences. Proc. Natl. Acad. Sci. USA 102, 6543-6549 (2005). 
3. West-Eberhard, M. J. Phenotypic Plasticity and the Origins of Diversity. Annu. 
Rev. Ecol. Syst. 20, 249-278 (1989). 
4. Pomiankowski, A. & Iwasa, Y. What Causes Diversity in Male Sexual 
Characters. Rev. Suisse Zool. 102, 883-893 (1995). 
5. Via, S. et al. Adaptive Phenotypic Plasticity - Consensus and Controversy. 
Trends Ecol. Evol. 10, 212-217 (1995). 
6. Pigliucci, M. Evolution of phenotypic plasticity: where are we going now? 
Trends Ecol. Evol. 20, 481-486 (2005). 
6 
7. Tregenza, T. Divergence and reproductive isolation in the early stages of 
speciation. Genetica 116, 291-300 (2002). 
8. González Zuarth, C. & Macías Garcia, C. Phenotypic differentiation and pre-
mating isolation between allopatric populations of Girardinichthys multiradiatus. Proc. 
R. Soc. Lond. B 273, 301-307 (2006). 
9. Joshi, A. Inbreeding and sex: canalization, plasticity and sexual selection. J. 
Genet. 84, 13-15 (2005). 
10. Endler, J. A. Natural selection on color patterns in Poecilia reticulata. Evolution 
34, 76-91 (1980). 
11. Endler, J. A. Variation in the appearance of guppy color patterns to guppies and 
their predators under different visual conditions. Vis. Res. 31, 587-608 (1991). 
12. Lachlan, R. F. & Servedio, M. R. Song learning accelerates allopatric speciation. 
Evolution 58, 2049-2063 (2004). 
13. Macías Garcia, C., Saborio, E. & Berea, C. Does male-biased predation lead to 
male scarcity in viviparous fish? J. Fish Biol. 53, 104-117 (1998). 
14. Coleman, S. W., Patricelli, G. L. & Borgia, G. Variable female preferences drive 
complex male displays. Nature 428, 742-745 (2004). 
15. Smith, C. B. & Martins, E. P. Display plasticity in response to a robotic lizard: 
Signal matching or song sharing in lizards? Ethology 112, 955-962 (2006). 
16. Patricelli, G. L., Coleman, S. W. & Borgia, G. Male satin bowerbirds, 
Ptilonorhynchus violaceus, adjust their display intensity in response to female startling: 
an experiment with robotic females. Anim. Behav. 71, 49-59 (2006). 
17. Olofsson, H. & Servedio, M. R. Sympatry affects the evolution of genetic versus 
cultural determination of song. Behav.l Ecol. 19, 594-604 (2008). 
7 
18 Endler, J. A. Signals, signal condition, and the direction of evolution. Am. Nat. 
139, s125-s153 (1992). 
19. Dewitt, T. J. Wilson, D. S. Costs and limits of phenotypic plasticity. Trends 
Ecol. Evol. 13, 77-81 (1998). 
20. Relyea, R. A. Cost of phenotypic plasticity. Am. Nat. 159, 272-282 (2002). 
 
We thank E. Avila and E. Tobón for considerable help in the field. This project was partially supported 
with a grant from CONACyT, and is part of C.G.Z.’s Ph.D. thesis. This research adhered to the 
Association for the Study of Animal Behaviour/Animal Behavior Society Guidelines for the Use of 
Animals in Research, local legislation and institutional code of conduct. 
Correspondence and requests for materials should be addressed to C. Gonzalez Zuarth 
(calbert@miranda.ecologia.unam.mx). 
8 
 
Table 1. A discriminant analysis based on the tendency to perform 
dynamic display behaviours classified accurately 40.70% of the males by 
their population of origin (F10,40= 2.708, p< 0.0001). Correct assignations 
are marked with bold characters. 
 Population in which males were classified  
Population 
of origin 
Porvenir Salazar Santiago San 
Juanico 
Zempoala 
Porvenir 6 0 2 3 1 
Salazar 0 5 1 4 0 
Santiago 2 1 3 6 0 
San Juanico 1 4 4 2 1 
Zempoala 0 0 1 1 6 
 
9 
 
Table 2. Cochran's Q tests showed that females differed systematically 
and significantly in their responses to homogametic and heterogametic 
males’ courtship. Each row shows the result of comparing the responses 
of females from each population (i.e. Zempoala in the first row) to 
heterogametic (Salazar in the first row) and to homogametic males. 
 Dynamic  display behaviours Static display behaviours 
Comparisons n(df) Q p N(df) Q p 
Zempoala Salazar 35(1) 5.00 0.025 8(1) 4.00 0.045 
Zempoala San Juanico 31(1) 8.00 0.005 14(1) 6.00 0.01 
Zempoala Porvenir 31(1) 11.00 0.000 14(1) 4.00 0.045 
Zempoala Santiago 35(1) 7.00 0.014 14(1) 6.00 0.014 
Salazar Zempoala 31(1) 9.00 0.003 14(1) 4.00 0.046 
Salazar San Juanico 35(1) 10.00 0.002 14(1) 6.00 0.01 
Salazar Porvenir 35(1) 9.00 0.003 14(1) 4.00 0.046 
Salazar Santiago 35(1) 7.00 0.008 14(1) 6.00 0.01 
San Juanico Zempoala 31(1) 12.00 0.001 14(1) 4.00 0.045 
San Juanico Salazar 31(1) 11.00 0.001 8(1) 4.00 0.045 
San Juanico Porvenir 35(1) 10.00 0.002 8(1) 1.00 0.317 
San Juanico Santiago 35(1) 15.00 0.000 14(1) 3.00 0.08 
Porvenir Zempoala 31(1) 5.00 0.02 14(1) 4.00 0.045 
Porvenir Salazar 35(1) 10.00 0.002 6(1) n.c n.c 
Porvenir San Juanico 31(1) 5.00 0.02 14(1) 4.00 0.045 
10 
Porvenir Santiago 35(1) 7.00 0.008 14(1) 3.00 0.08 
Santiago Zempoala 31(1) 6.00 0.01 14(1) 1.00 0.317 
Santiago Salazar 35(1) 7.00 0.058 14(1) 1.00 0.317 
Santiago San Juanico 31(1) 7.00 0.008 14(1) 3.00 0.083 
Santiago Porvenir 35(1) 8.00 0.005 8(1) 3.00 0.083 
 
11 
 
Table 3. Planned comparisons showed that males modified their courtship 
pattern when they were exposed to heterogametic females. 
Males population Females population F p 
Porvenir Salazar F(4,45)=11.560 0.001 
Porvenir Santiago F(4,45)=5.841 0.019 
Porvenir San Juanico F(4,45)=17.586 0.000 
Porvenir Zempoala F(4,45)=7.754 0.007 
Salazar Porvenir F(4,36)=1.288 0.264 
Salazar Santiago F(4,36)=4.387 0.043 
Salazar San Juanico F(4,36)=3.302 0.077 
Salazar Zempoala F(4,36)=5.979 0.019 
Santiago Porvenir F(4,48)=5.434 0.024 
Santiago Salazar F(4,48)=4.184 0.046 
Santiago San Juanico F(4,48)=12.428 0.000 
Santiago Zempoala F(4,48)=0.609 0.439 
San Juanico Porvenir F(4,44)=0.098 0.755 
San Juanico Salazar F(4,44)=4.822 0.033 
San Juanico Santiago F(4,44)=1.933 0.171 
San Juanico Zempoala F(4,44)= 4.201 0.045 
Zempoala Porvenir F(4,27)=3.903 0.058 
Zempoala Salazar F(4,27)= 7.022 0.013 
12 
Zempoala Santiago F(4,27)=5.418 0.027 
Zempoala San Juanico F(4,27)=7.850 0.009 
 
13 
 
 


Courtship plasticity reveals the evolution of dialects in allopatric fish populations

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Courtship plasticity reveals the evolution of dialects in allopatric fish populations

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