Selection in sympatric populations of Cepaea

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Selection in sympatric populations of Cepaea

L.I. Mazon, M.A. Martinez de Pancorbo, A. Vicario, A.I. Aguirre, A.

Estomba, C.M. Lostao

To cite this version:

Original

Selection

in

_sympatric

_populations

of

_Cepaea

L.I. Mazon1 M.A. Martinez de Pancorbo A. Vicario A.I.

_Aguirre

₁

1 Universida

d de1 Pais _{Vasco, faculdad} de _{ciencias, departamento} de _biologia y genetica,

APDO, 6!, 48080

2

Universidad del Pais _{Vasco, faculdad} de _{medíci!a, departamento} de _histologia y biologia,

l,8080, Spain

(received 16 _{May 1988, accepted} 30 January 1989)

Summary - Interspecific competition is often _thought to _{produce evolutionary changes.}

This _competition has been studied _{mainly, using subjects} whose _heritability is not well known. Hence it is _preferable to _{study polymorphic} characters whose inheritance is known.

Land snails of the _{genus Cepaea} have several _advantages for such studies.

Ninety-five samples of allopatric and _{sympatric populations} of Cepaea ne!n,orn.lis and Cepaea hortensis were collected near the southern limit of the aera occupied by Cepaea

hortensis. In the area _{studied, Cepaea} nemoralis and _Cepaea hortensis _populations are

divided into two zones _{corresponding} to the north and _south-facing slopes of the Iberian Mountains.

Changes in _{phenotype frequencies} were observed _passing from _allopatry to _sympatry in both species. In the _North, a decrease in the _frequencies of _{yellow, yellow-banded} and

effectively banded _yellow snails was detected in _{sympatric populations} of _Cepaea nemoralis and, at the same time, the _frequencies of the _{banded, five-banded,} and _effectively banded

phenotypes in _Cepaea hortensis increased. These _changes in _{phenotype frequencies} between allopatric and sympatric populations in one species _may depend _upon the phenotype

frequency of the other. Such _{frequency dependent} selection may interact with other

selective forces and with _competitive selection.

We believe _that, in southern _populations, these _changes are due to climatic selection in both _species.

Cepaea - polymorphism - climatic selection - allopatry - sympatry

Résumé - Sélection dans les populations sympatriques de Cepaea. La _compétition interspécifique produit des _{modifications} évolutives. Cette _compétition a été étudiée surtout

sur des caractères dont d’hérédité était mal connue. Comme il est _préférable d’utiliser des caractères dont l’hérédité est _établie, les _escargots du genre Cepaea constituent un bon

modèle pour ces recherches. On a _prélevé 95 échantillons de populations allopatriques

et _sympatriques de _Cepaea nemoralis et de _Cepaea hortensis à _proximité de l’extrémité méridionale de l’aire d’extension de _Cepaea hortensis. Dans l’aire de la _{présente étude,} les _populations de _Cepaea nemoralis et de _Cepaea hortensis sont _séparées en deux zones

correspondant aux versants méridionaux et _{septentrionaux} des montagnes ibériques. On

a observé des variations de _{fréquences phénotypiques,} en _passant de _{l’allopatrie} à la

et _{jaune efj’ectivement bandé,} et _{simultanément,} chez _{Cepaea hortensis,} un accroissement des _fréquences des phénotypes bandé, cinq-bandé, et _{ejj’ectivement} bandé. Ces variations

de _{fréquences phénotypiques} observées dans une _espèce entre des _{populations allopatriques}

et _{sympatriques peuvent dépendre} des _{fréquences phénotypiques} dans l’autre _espèce. Cette

sélection _dépendant de la _{fréquence peut interagir} avec d’autres _forces sélectives et avec

la sélection _{compétitive.} Les variations observées ici dans les _populations méridionales semblent dues à la sélection _climatique dans les deux espèces.

Cepaea - polymorphisme - sélection climatique - allopatrie - sympatrie

INTRODUCTION

Cepaea nemoralis and _Cepaea hortensis are two _closely related and _{morphologically} similar _{species (Lamotte, 1951).} Each _presents a _very similar polymorphism with the same _patterns of colour and _banding of _shell, and they frequently form mixed

populations.

The range of these two _{species overlaps.} In Northern Europe, Cepaea hortensis reaches _{higher latitudes,} while _Cepaea nemoralis reaches more _southerly latitudes.

This may indicate that _Cepaea hortensis is more resistant to cold climates than

Cepaea nemoralis, which in _turn, is better _adapted to milder climates

_(Cameron,

In mixed _populations, different _{morph frequencies} are often found for each

species, and some local correlations have also been found between _morphs of the two. This could be due to several factors: to visual selection on shell _pattern or

size _{(Clarke, 1960, 1962a, b; Carter, 1967;} Bantock & _{Bayley, 1973;} Bantock et

al., 1976); to _{interspecific competition (Arthur, 1978, 1980);} to climatic selection

(Arthur, 1982a) or to _{interspecific competition} and intra and _{interspecific} effects of

population density (Cameron & _{Carter, 1979).}

Various modes of _{evolutionary change resulting} from _{interspecific competition} have been _proposed: character _{displacement (unilateral} or _{bilateral), convergence}

of characters and alteration of the variance of _{morphological characters,} evolution of _{competitive capacity} and _{&dquo;genetic} feedback&dquo; _{(Arthur, 1982b).}

Here, we _{study populations} of _Cepaea nemoralis and _Cepaea hortensis in

allopa-try and _sympatry, to _analyse whether climatic selection or _{interspecific competition} cause _any differences between _allopatric and _{sympatric populations.} We study them

in a zone where _Cepaea hortensis is at the _{edge of its range. Marginal populations}

are _interesting since _they may be found in limiting environmental or _competitive

conditions _(Bantock & _{Price, 1975).}

MATERIAL AND METHODS

Sampling was carried out in the western _part of the Iberian Mountains _{(Fig. 1).} This zone has _high peaks (San Lorenzo 2,262 meters, Picos de Urbion 2,228 meters,

etc.) and _{deep valleys.} It is very cold in winter and hot in summer. Each _sample

A total of 7 235 snails was collected, of which 5 220 were _Cepaea nemoralis

and 2 015 were _Cepaea hortensis. _{Fifty allopatric} and 32 sympatric populations were found for Cepaea nemoralis (Table I), while for Cepaea hortensis, there were

13 _allopatric and 32 _sympatric. For _{the purpose of analysis, only} 23 _sympatric

populations of nemoralis and 26 of hortensis were considered. The difference in the

number of sympatric populations of the two _species is due to the fact that some

populations had a very small number of individuals. Samples were scored according to the criteria of Lamotte _(1951), Cain and _{Sheppard (1954)} and Arnold

_(1968).

For each _sample, data on _{vegetation, pH,} soil characteristics, climate, distance from

the sea and altitude were collected.

RESULTS

Cepaea nemoralis is more common and more widespread, than is Cepaea hortensis.

Each _species is _polymorphic in the _region. For _{Cepaea nemoralis,} the area _sampled was divided into _{two zones,} the north and _{south-facing slopes} of the Iberian Mountains _{(Table II). Phenotype} differences _{appeared, principally} in the patterns

of bands _{(Fig. 2), whereas,} for _coloured, no differences were _apparent.

We examined _allopatric and _{sympatric populations} in each zone. In the southern zone there were no _significant differences in either _species. In the _{north-facing slopes,}

allopatric populations of _Cepaea nemoralis _exhibit, a significant increase in _yellows,

banded _yellows and _effectively banded yellows (Table II), while in the _sympatric

zone the _pinks are more frequent.

In _{allopatric populations} of _{Cepaea hortensis,} unbanded _{yellow, effectively}

un-banded and unbanded _phenotypes were _{significantly} more _frequent than _in

sym-patric populations, while in the _{latter, effectively banded,} banded and _yellow 12 345

were more _frequent in the northern zone _(Table

_II).

When _frequencies are _compared between _species in _sympatry and in _allopatry in each _zone, the number of _significant differences are much the same for allopatric and

sympatric comparisons in the south. In the _{north, however, allopatric comparisons}

There were no _significant differences of _phenotypic frequencies related to soil

characteristics, pH or _{vegetation. However,} there were _significant differences in the

altitude of _populations between northern and southern _{slopes (Table}

_III).

There was a series of significant correlations (P < _0.05) between _morph frequen-cies and altitude in _{Cepaea hortensis,} but not with very high correlation coefficients.

In the northern _zone, the unbanded _yellow and _effectively unbanded _yellow

pheno-types were _positively correlated with altitude. In the southern _zone, yellow 12 345

and 12 345 were _{negatively correlated, whereas,} fusion-yellow and fusion-banded were _positively correlated. _Cepaea nemoralis _{phenotypes, positively} correlated with

altitude, include _pink 00300 and _yellow 00300 in the North.

Trush _predation was found in _only five _populations, of which, three were

allopatric and the other two, sympatric (Table IV). In two _populations, the

predation is not _selective, and in the _remaining three, the most _{heavily predated} are the fusion banded or effectively banded for Cepaea nemoralis,

(San

banded shells,

X3

=

_xi

ki =

x3 =

In our _study, each _population is _composed of 16 different _{phenotypes. Up} to now,

we have made _{comparison phenotype by phenotype.} This _gives an idea of what is

happening with _just one phenotype at a time in each _species, but causes a loss of

perspective with _respect to what is _occurring overall. _Therefore, we looked for an

analysis where the 16 _phenotypes and all the _populations could be introduced, and whose results would be _easy to _interpret; an _analysis which fulfills all these demands

is Factorial _{Correspondence Analysis (FCA).}

Two _{large groups} of _Cepaea nemoradis and _Cepaea hortensis were _separated (Fig.

3),

grouped into two different areas in the figure. Within Cepaea _nemoralis, there was a

subgroup including the _{sympatric populations, although} in this case, the separation

was not as clear as between _species.

FCA _{represents phenotypes} and _populations and also _keeps the _proximity

relationship (i.e. the _Cepaea hortensis _populations are close to _{phenotypes yellow}

12 345, fusion banded _yellow and _{hyalozonate),} which indicates _that, in _Cepaea

hortensis, these are the most _{frequent phenotypes.}

This _separation may also be observed in the cluster

(Fig. 4),

neighbour/paired

at 0.165 with a _{high proportion} of unbanded _yellow. For _{Cepaea nemoralis,} there

is a _group at _0.102, where the _majority of _populations are _allopatric.

DISCUSSION AND CONCLUSIONS

In our _{area, Cepaea} nemoralis _populations seem to be divided into two zones

corresponding to the north and _{south-facing slopes} of the Iberian Mountains.

Marked climatic differences characterize the two zones. The southern zone is drier

and hotter with more severe climatic conditions than in the northern zone. The

observed differences in the _{phenotype frequencies} could be _{produced by} climatic selection or _{by geographic isolation,} due to the Iberian Mountains.

When _analysing the _passage from _allopatry to _sympatry within each _species,

changes may be observed in the frequencies of colour patterns and shell _banding. On _{north-facing slopes} of the Iberian _Mountains, in _{sympatric populations} of _Cepaea nemoralis, the _effectively banded _yellows and other _{yellow morphs} decreased. With

regards to colour, pink shells increased in _sympatry, while _{yellow phenotypes} decreased. For _{Cepaea hortensis,} the banded _phenotypes also increased in _sympatric

1982a) observations. _{The gene} for shell colour of _Cepaea hortensis does not seem

to be affected.

Why are there such _frequency differences between _allopatric and _sympatric

populations? Some authors have _proposed visual selection as the main cause

(Clarke,

to be _so, since trush _predation is very slight, and not _significant. Others authors

have _{suggested interspecific (Arthur, 1978, 1980)} or climatic selection _(Cameron, 1970 _{a, b, c, Arthur, 1980), although} it is _very difficult to _separate the two _(Arthur, 1982a). Climatic selection _may be _important in our southern populations, as there are no differences between the _{morph-frequencies} of the _allopatric or the _sympatric

populations within a _species, while in the north there are differences. Another

argument in favour of this kind of selection, is that the _Cepaea hortensis _populations

sampled are _marginal, and _may be in _{environmentally limiting} conditions. Moreover,

the _{sympatric populations} of Cepaea hortensis in the southern zone are significantly

higher in altitude than those in the north, as _happens with _{allopatric populations}

of _Cepaea nemoralis.

For _sympatry, there are more _significant differences between the two _species in the _north, than in the south. _However, for _{allopatry, they} are _higher in the south.

Allopatric populations present more differences in _{morph-frequencies probably} due

to differences in niches or _{adaptative strategies.} It is known that _Cepaea nemoralis and _Cepaea hortensis have different _strategies to reach similar _darkening of the shell

(Jones et _{al., 1977).}

In the northern _zone, the _{allopatric populations} in both species have few

signif-icant differences in their _{morph-frequencies.} That _implies that there is little effect of climatic selection on the northen _slopes, with a _{greater importance} of

interspe-cific _competition, since the differences between _species increase in _sympatry. The

phenotypes of _Cepaea nemoralis or _{Cepaea hortensis,} which _{present significant}

dif-ferences between _allopatry and _sympatry, would suffer _{interspecific competition.} A

possible strategy would be _displacement of _{morph-frequencies} towards _phenotypes

infrequent in the other _{sympatric species,} in an _attempt to make the two _species

ap-pear very different as far as their phenotype frequencies are concerned

(i.e.,

the _phenotypes which suffer _{displacement,} if one _species has _{high frequencies} of a

phenotype, the other _species tends to decrease its _frequency when it _passes from

al-lopatry to _sympatry, thus _increasing the differences between the _{morph-frequencies} of both _species). This is reflected in the FCA _{(Fig. 3),} where _{sympatric populations} of _Cepaea nemoralis appear on _average farther from _Cepaea hortensis than _allopatric

populations. Also _{sympatric populations} of C. hortensis appear, on _average, farther

from C. nemoralis than the _{allopatric populations, although genetic} flow between

same _{species populations may} exist. _However, Cowie and Jones ₍₁₉₈₇₎ showed that there is _competition and habitat _separation in _Cepaea, but found no evidence of

an _{interspecific} interaction that _might be a _precursor of character displacement in

experimentally mixed _population of C. nemoradis and C. hortensis. _They consider

that the _{competition may} reflect a balance between invasion and extinction. On the

other _hand, Arthur _(1982a) observed differences between _allopatry and sympatry,

possibly due to climatic _factors, since _{allopatric populations} of _Cepaea nemoralis

(1984), also show differences in wooded habitats. In our study, we did not observe

such a difference.

This leads us to believe _that, in the _south, the _limiting factor is _climatic, while in the north, there may be a mixture of climatic factors and _{competitive displacement.}

Taking into account these results, climatic selection may be acting upon one or

both _species and _competitive selection can be detected in the _species or _phenotypes not _subject to climatic _{selection, although} it is not clear whether there is an

interaction between the two.

We _{agree with} Arthur _(1982a), that there is no reason _why unbandeds should be weaker _{interspecific competitors,} or why climatic selection should be the cause of the

frequency changes when _passing from _allopatry to _sympatry. We think rather, that

a phenotype will be a _stronger or weaker _{competitor depending} on the frequency it

has in the other _species. This is an extension of the _concept of selection _depending

on _frequencies to a two _species situation _{(see Arthur, 1982b). Frequency dependent} selection had _already been noted for mixed _colonies, but from the _point of view of

selection _{(Clarke, 1962b,} Bantock et _{al., 1976).} There are cases where differences

have not been observed in _{morph-frequencies} between _allopatric and sympatric

populations; this may be due to interaction between various selective forces which

neutralise character _{displacement,} or to an _equilibrium in the mixed populations.

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