TRENDS in Ecology & Evolution Vol.16 No.

7 J uly 2001
http://tree.trends.com01695347/01/$ see front matter 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02198-X
372 Review
Dolph Schluter
Zoology Dept and The
Center for Biodiversity
Research, The University
of British Columbia,
Vancouver, BC, Canada
V6T 1Z4.
e-mail:
schluter@zoology.ubc.ca
ECOLOGI CAL SPECI ATI ON (see Gl ossary) occurs when
DI VERGENTSELECTI ON on trai ts between popul ati ons or
subpopul ati ons i n contrasti ng envi ronments l eads
di rectl y or i ndi rectl y to the evol uti on of REPRODUCTI VE
I SOLATI ON. The concept of ecol ogi cal speci ati on dates
back to the 1940s, from the ti me the BI OLOGI CAL SPECI ES
CONCEPTwas devel oped. Dobzhansky
1
bel i eved that
SPECI ATI ON i n Drosophilaproceeds mai nl y through
evol vi ng physi ol ogi cal compl exes whi ch are successful
each i n i ts envi ronment. Mayr
2
recogni zed that many
of the accumul ated geneti c di fferences between
popul ati ons parti cul arl y those affecti ng physi ol ogi cal
and ecol ogi cal characters, are potenti al i sol ati ng
mechani sms. Acceptance of thi s perspecti ve by many
evol uti oni sts i n the mi d-20th century resul ted from
the i nherent appeal and si mpl e pl ausi bi l i ty of
ecol ogi cal speci ati on. However, unti l recentl y, nei ther
was there evi dence to support ecol ogi cal speci ati on,
nor had tests been devi sed and appl i ed to di sti ngui sh
ecol ogi cal speci ati on from other mechani sms that
mi ght al so cause speci ati on i n the wi l d, such as
GENETI C DRI FT(BOX 1).
Mechanisms of ecological speciation
Ecol ogi cal speci ati oni s a concept that uni tes
speci ati on processes i n whi ch reproducti ve i sol ati on
evol ves ul ti matel y as a consequence of di vergent
(i ncl udi ng DI SRUPTI VE) sel ecti on on trai ts between
envi ronments. Envi ronmentrefers to bi oti c and
abi oti c el ements of habi tat (e.g. cl i mate, resources
and physi cal structure) as wel l as to i nteracti ons wi th
other speci es (e.g. resource competi ti on, predati on,
mutual i sm and vari ous forms of i nterspeci fi c
i nterference). A di versi ty of evol uti onary processes
mi ght be i nvol ved. Ecol ogi cal speci ati on mi ght occur
i n ALLOPATRY or i n SYMPATRY. I t mi ght l ead to mai nl y
premati ng i sol ati on, mai nl y postmati ng i sol ati on, or a
combi nati on of both. I t i ncl udes several (but not al l )
modes of speci ati on i nvol vi ng SEXUAL SELECTI ON.
Ecol ogi cal speci ati on mi ght come about i ndi rectl y as a
consequence of natural sel ecti on on morphol ogi cal ,
physi ol ogi cal or behavi oral trai ts, or i t mi ght i ncl ude
di rect sel ecti on on premati ng i sol ati on
(REI NFORCEMENT). Di sti ngui shi ng the ways i n whi ch
di vergent sel ecti on has l ed to reproducti ve i sol ati on i s
among the greatest chal l enges of the empi ri cal study
of ecol ogi cal speci ati on.
I n what i s perhaps the cl assi c scenari o for
ecol ogi cal speci ati on (Fi g. 1), reproducti ve i sol ati on
between two popul ati ons starts to bui l d i n al l opatry as
popul ati ons accumul ate adaptati ons to uni que aspects
of thei r envi ronments. Premati ng i sol ati on then
evol ves to compl eti on by rei nforcement after sympatry
i s secondari l y establ i shed. The ti mi ng of SECONDARY
CONTACTi s fl exi bl e, however, and the extremes of
possi bi l i ty l ead to departures from thi s cl assi c model .
At one extreme i s pure ALLOPATRI C SPECI ATI ON, i n whi ch
the sympatri c phase i s enti rel y absent. New speci es
mi ght eventual l y become sympatri c, but thi s occurs
after reproducti ve i sol ati on i s compl ete. The other
extreme i s ful l -bl own SYMPATRI C SPECI ATI ON, whi ch
compl etel y l acks the al l opatri c stage. Al though debate
about the pl ausi bi l i ty of these extremes has l ong
pol ari zed research on speci ati on, from an ecol ogi cal
perspecti ve, the more fundamental i ssue concerns the
mechani sms that dri ve the evol uti on of reproducti ve
i sol ati on, whi ch i s the focus of thi s arti cl e.
By-product mechanisms
I n the si mpl est model s of ecol ogi cal speci ati on,
reproducti ve i sol ati on bui l ds between popul ati ons
i nci dental l y as a by-product of adaptati on to
al ternati ve sel ecti on regi mes
2,3
. Reproducti ve
i sol ati on i s not di rectl y favored by sel ecti on, but i s a
secondary consequence of geneti c di fferenti ati on
dri ven by sel ecti on on other trai ts. Thi s BY-PRODUCT
MECHANI SM coul d l ead to premati ng i sol ati on and to
vari ous forms of postmati ng i sol ati on.
Several l aboratory experi ments wi th Drosophila
have si mul ated the earl y stages of by-product
speci ati on (revi ewed i n Ref. 4), and these hi nt at how
the process mi ght work i n nature. Ki l i as et al.
5
rai sed
di fferent l i nes of Drosophila melanogaster for fi ve
years i n ei ther a col ddrydark or a
warmdampl i ght envi ronment. Dodd
6
exami ned
mati ng preferences i n repl i cate l i nes of Drosophila
pseudoobscurarai sed for one year on ei ther starch-
based or mal tose-based l arval medi um. I n both
studi es, some premati ng reproducti ve i sol ati on
evol ved between l i nes that had experi enced
contrasti ng envi ronments, but no premati ng i sol ati on
evol ved between i ndependent l i nes rai sed i n the same
envi ronment (Fi g. 2). The popul ati ons i n these
experi ments were ful l y al l opatri c, as i n the fi rst part
of the cl assi c scenari o (Fi g. 1).
The ecological hypothesis of speciation is that reproductive isolation evolves
ultimately as a consequence of divergent natural selection on traits between
environments.Ecological speciation is general and might occur in allopatry or
sympatry,involve many agents of natural selection,and result from a
combination of adaptive processes.The main difficulty of the ecological
hypothesis has been the scarcity of examples from nature,but several potential
cases have recently emerged.I review the mechanisms that give rise to new
species by divergent selection,compare ecological speciation with its
alternatives,summarize recent tests in nature,and highlight areas requiring
research.
Ecology and the origin of species
Dolph Schluter
However, compl ete al l opatry i s not cruci al for the
by-product mechani sm, an i dea that extends the cl assi c
scenari o i n two ways
4
. Fi rst, sel ecti on can conti nue to
strengthen reproducti ve i sol ati on vi a the by-product
mechani sm even when the al l opatri c phase i s over and
the sympatri c phase i s i n progress. Rei nforcement i s
not the onl y way to compl ete the evol uti on of
reproducti ve i sol ati on after secondary contact. Second,
TRENDS in Ecology & Evolution Vol.16 No.7 J uly 2001
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373 Review
Speciation modes have been classified
historically by the geographical
arrangement of populations undergoing the
process (allopatric, sympatric or parapatric),
a classification that focuses on the inhibitory
effects of gene flow on the evolution of
reproductive isolation. Some have argued
that an alternative classification centering
on mechanisms that drive the evolution of
reproductive isolation would be more
productive
ac
(Via
d
, this issue). TableI breaks
modes of speciation events into four
categories according to initial cause, and
compares some other principal features of
those categories.
Natural selection is involved at an early
stage of two different modes of speciation.
Under ecological speciation, populations in
different environments, or populations
exploiting different resources, experience
contrasting natural selection pressures on
traits that directly or indirectly bring about
the evolution of reproductive isolation.
However, divergence might also occur
under uniform selection, for example, if
different advantageous (but incompatible)
mutations arise in separate populations
occupying similar environments (Turelli et al.
e
,
this issue). Reproductive isolation between
populations brought about by conflict and
coevolution between the sexes within
populations
fh
is an example of this second
mode.
If populations are in contact before the
evolution of reproductive isolation is
completed, natural selection might be
involved at a late stage of all four modes of
speciation, during reinforcement of
premating isolation (Turelli etal.
e
this
issue)
i
. Similarly, sexual selection might be
involved in every speciation mode,
depending on the cause of divergence in
mate preferences. For this reason, the
presence of natural or sexual selection
per se is probably not a good basis for
classifying speciation events. Nevertheless,
the classification in Table I is coarse, and
finer subdivisions are necessary to highlight
differences in the roles of natural and sexual
selection within each mode, as well as
different roles for genetic drift in speciation
initiated by that mechanism.
References
a Schl uter, D. (1996) Ecol ogi cal speci ati on i n
postgl aci al fi shes. Philos. Trans. R. Soc. London
Ser. B 351, 807814
b Schl uter, D. (1998) Ecol ogi cal causes of
speci ati on. I n Endless Forms: Species and
Speciation(Howard, D. and Berl ocher, S., eds),
pp. 114129, Oxford Uni versi ty Press
c Orr, M.R. and Smi th, T.B. (1998) Ecol ogy and
speci ati on. Trends Ecol. Evol. 13, 502506
d Vi a, S. (2001) Sympatri c speci ati on i n ani mal s:
the ugl y duckl i ng grows up. Trends Ecol. Evol.
16, 381390
e Turel l i , M. et al. (2001)Theory and speci ati on.
Trends Ecol. Evol. 16, 330343
f Pal umbi , S.R. (1998) Speci es formati on and the
evol uti on of gamete recogni ti on l oci . I n Endless
Forms: Species and Speciation(Howard, D. and
Berl ocher, S., eds), pp. 271278, Oxford
Uni versi ty Press
g Ri ce, W.R. (1998) I ntergenomi c confl i ct,
i nterl ocus antagoni sti c coevol uti on, and the
evol uti on of reproducti ve i sol ati on. I n Endless
Forms: Species and Speciation(Howard, D. and
Berl ocher, S., eds), pp. 261270, Oxford
Uni versi ty Press
h Gavri l ets, S. (2000) Rapi d evol uti on of
reproducti ve i sol ati on dri ven by sexual confl i ct.
Nature403, 886889
i Dobzhansky, T. (1951) Genetics and theOrigin
of Species(3rd edn), Col umbi a Uni versi ty Press
Box 1.The major modes of speciation,according to initial causes
Table I.Modes of speciation
Mode of speciation Mechanism of initial Initial form of Proximate basis of Examples of the roles of Example roles of
divergence reproductive reduced hybrid natural selection sexual selection
isolation fitness
Ecological speciation Divergent natural Prezygotic or Ecological selection, Initial: Drive divergence in Amplify
selection postzygotic genetic incompatibility phenotypic traits divergence of
and sexual Final: Reinforcement mate preferences
incompatibility initiated by
natural selection
Reinforcement
Speciation by Different advantageous Prezygotic or Genetic incompatibility Initial: Drive fixation of Drive fixation of
divergence under mutations occur in postzygotic and sexual incompatible mutations alternative
uniform selection separate populations incompatibility in different populations incompatible
experiencing similar Final: Reinforcement mutations in
selection pressures different
populations
Reinforcement
Speciation by Genetic drift Prezygotic or Genetic incompatibility Initial: None; or opposes Amplify
genetic drift postzygotic and sexual divergence differences in
incompatibility Final: Reinforcement mate preferences
caused by drift Reinforcement
Polyploid speciation Hybridization and Postzygotic Genetic incompatibility Initial: None; or promotes Reinforcement
polyploidy further genetic divergence
Final: Reinforcement
an i ni ti al al l opatri c phase i s not al ways essenti al for
the by-product mechani sm to work, and can be
di spensed wi th i f sel ecti on i s strong enough or i f gene
fl ow between subpopul ati ons i s not too hi gh (see Turel l i
et al.
7
, thi s i ssue, and Vi a
8
, thi s i ssue).
Many di fferent envi ronmental agents of di vergent
sel ecti on coul d l ead to the evol uti on of reproducti ve
i sol ati on as a by-product, and i denti fyi ng these
al ternati ves i s of major i nterest. Duri ng the al l opatri c
phase, such agents mi ght i ncl ude contrasti ng
resources, predators, competi tors, cytopl asmi c
symbi onts, structural habi tat features affecti ng
l ocomoti on or transmi ssi on of communi cati on si gnal s,
and other bi oti c and abi oti c factors. Al l opatri c
popul ati ons mi ght al so confront di sti nct
constel l ati ons of other cl osel y rel ated speci es, whi ch
coul d l ead to di vergence of mati ng and soci al si gnal s i f
these si gnal s evol ve partl y i n response to i nterspeci fi c
i nterference. The l ast mechani sm extends the by-
product concept to di vergence i n a wi der set of trai ts,
such as col or and song, than those i mmedi atel y
rel ated to resource acqui si ti on. For exampl e,
di vergence of col or i n response to i nterspeci fi c
reproducti ve or aggressi ve i nterference wi th other
speci es coul d expl ai n the rapi d di vergence of sexual
si gnal s and mate preferences between spati al l y
separated popul ati ons of Afri can ci chl i d fi sh that are
otherwi se si mi l ar i n food and habi tat requi rements
9,10
(see Barracl ough and Nee
11
, thi s i ssue).
Many agents of di vergent sel ecti on that dri ve the
evol uti on of reproducti ve i sol ati on between two
al l opatri c popul ati ons woul d conti nue to strengthen
i sol ati on fol l owi ng secondary contact. However, other
agents of sel ecti on that ari se from i nteracti ons
between the two nascent speci es are added duri ng the
sympatri c phase, and these too mi ght dri ve
reproducti ve i sol ati on to compl eti on. For exampl e,
competi ti on for resources between sympatri c
popul ati ons coul d l ead to exaggerated di vergence i n
phenotype, and further enhance reproducti ve
i sol ati on as a by-product. Al ternati vel y, di vergent
sel ecti on coul d generate body si ze di fferences that
resul t i n predati on on the smal l er speci es by
i ndi vi dual s of the l arger. Any evol uti on of behavi oral
defenses i n the smal l er speci es woul d probabl y reduce
the frequency of crossbreedi ng as a by-product. Thi s
l ast mechani sm was rai sed as a possi bl e expl anati on
for enhanced premati ng i sol ati on between a pai r of
threespi ne sti ckl eback Gasterosteusspp. i n whi ch
femal es of the l arger speci es prey upon eggs guarded
by mal es of the smal l er speci es
12
. The i nfl uence of
such i nteracti ons on the evol uti on of reproducti ve
i sol ati on duri ng the sympatri c phase of speci ati on has
recei ved very l i ttl e attenti on.
Reinforcement and sympatric speciation
Di vergent natural sel ecti on i n the al l opatri c phase
mi ght bui l d up di fferences l eadi ng to reduced hybri d
fi tness after secondary contact that subsequentl y
favor rei nforcement
3,13
. Rei nforcement i s di sti nct
from the by-product mechani sm because sel ecti on
di rectl y favors enhanced premati ng i sol ati on as a
consequence of the i nferi ori ty of hybri d offspri ng.
Dobzhansky
3
vi ewed rei nforcement as domi nati ng
the compl eti on of ecol ogi cal speci ati on after
secondary contact (Fi g. 1), a cl ai m that remai ns to be
proven. Of course, rei nforcement mi ght occur even i n
non-ecol ogi cal speci ati on (Box 1). Consequentl y,
testi ng ecol ogi cal speci ati on requi res the exami nati on
of processes acti ng at an earl i er stage (e.g. duri ng the
al l opatri c phase).
Most concepti ons of sympatri c speci ati on i nvoke a
process si mi l ar to that of rei nforcement, except that
there i s no previ ous bui l d up of phenotypi c and geneti c
di fferences l eadi ng to l owered hybri d fi tness. I nstead,
the fi tness of i ntermedi ates of a si ngl e popul ati on i s
reduced from the start by di rect ecol ogi cal sel ecti on
pressures. For exampl e, i ntermedi ate phenotypes
(i ncl udi ng hybri ds) mi ght expl oi t avai l abl e resources
l ess effecti vel y than do extreme phenotypes
14,15
, or
i ntermedi ate phenotypes mi ght suffer greater overal l
resource competi ti on
16
. Doebel i and Di eckmann
17
have argued that sel ecti on agai nst i ntermedi ate
phenotypes i s the expected outcome of many types of
ecol ogi cal i nteracti ons, i ncl udi ng competi ti on, shared
predati on and shared mutual i sm (see al so Ref. 18)
and, under certai n condi ti ons, these mi ght favor the
evol uti on of premati ng reproducti ve i sol ati on i n
sympatry (see Vi a
8
, thi s i ssue).
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374 Review
TRENDS in Ecology & Evolution
Level of reproductive isolation
Allopatric phase Sympatric phase
0% 100%
By-product mechanism Reinforcement
Dominant mechanism assumed
Fig. 1. The classic
scenario of an ecological
speciation event, from
beginning to end.
Reproductive isolation
builds in allopatry (green)
as an incidental by-
product of adaptation to
alternative environments
(by-product mechanism).
Reinforcement of
premating isolation,
driven by reduced hybrid
fitness, completes the
speciation process during
the sympatric phase
(blue). The timing of
secondary contact is
flexible (indicated by
arrows at the boundary
between the allopatric and
sympatric phases).
TRENDS in Ecology & Evolution
P
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m
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s
0.2
0.3
0.4
0.5
0.6
Different Same
Type of environment
Fig. 2. Mating
compatibility of
independent experimental
lines of Drosophila raised
separately over multiple
generations in similar or in
different environments.
Circles represent the
proportion of mating
events that occurred
between individuals
from different lines
relative to intra-line
matings. Data are from
D. pseudoobscura
6
(green symbols) and
D. melanogaster
5
(blue symbols). Modified
from a figure to be
published by Cambridge
University Press (Ref. 64).
Ecology and sexual selection
Sexual sel ecti on i s regarded as a potent force dri vi ng
the evol uti on of premati ng and/or postmati ng i sol ati on
between popul ati ons (see Panhui s et al.
19
, thi s i ssue).
From an ecol ogi cal perspecti ve, the key questi on i s
how di vergent mate preferences become establ i shed i n
the fi rst pl ace. I n most theoreti cal model s of speci ati on
by sexual sel ecti on, di vergent natural sel ecti on pl ays a
domi nant rol e, as spati al vari ati on i n sel ecti on on
SECONDARY SEXUAL TRAI TS
20
, as di vergent sel ecti on on
sensory systems
21
, or as di fferences between
envi ronments i n the most effecti ve modes of mati ng
si gnal transmi ssi on
22,23
. By contrast, geneti c dri ft
24
or
uni que mutati ons favored by i ntersexual confl i ct
25,26
pl ay the domi nant rol e i n the evol uti on of reproducti ve
i sol ati on i n non-ecol ogi cal model s of speci ati on by
sexual sel ecti on. Therefore, a demonstrati on that
sexual sel ecti on i s i nvol ved i n the speci ati on process
does not, by i tsel f, restri ct the range of speci ati on
model s under i nvesti gati on (Box 1). The mechani sms
ul ti matel y dri vi ng di vergence of mate preference, i n
parti cul ar the rol e of di vergent natural sel ecti on, must
sti l l be i denti fi ed.
Tests of ecological speciation
Tests of ecol ogi cal speci ati on must consi der the
al ternati ves that need to be di sti ngui shed (Box 1):
speci ati on by ordi nary geneti c dri ft or geneti c dri ft
duri ng popul ati on BOTTLENECKS
27,28
; speci ati on by
fi xati on of al ternati ve advantageous genes i n
popul ati ons experi enci ng si mi l ar sel ecti on
pressures
29
; and speci ati on by pol ypl oi dy
30,31
.
Speci ati on by pol ypl oi dy can be readi l y di agnosed
geneti cal l y, but al though i t i s more common i n
pl ants than ani mal s, pol ypl oi dy accounts for onl y
24% of pl ant speci ati on events
32
. Even i n pl ants,
the cause of most speci ati on events remai ns to be
i denti fi ed.
Several tests have been carri ed out i n recent
years that i ndi cate a rol e for di vergent sel ecti on i n
the ori gi n of speci es i n nature (Tabl e 1).
Demonstrati ng a rol e for di vergent sel ecti on i n
speci ati on, however, i s onl y the fi rst step to detecti ng
an ecol ogi cal speci ati on event. The next step i s to
understand the process by whi ch di vergent sel ecti on
has l ed to the evol uti on of reproducti ve i sol ati on
(e.g. by-product al one or wi th rei nforcement,
mechani sms of hybri d fi tness, etc.), a step i n whi ch
l ess progress has been made. I have not revi ewed
evi dence from mol ecul ar studi es that i nfer natural
sel ecti on from an unusual l y hi gh rate of sequence
di vergence between si ster speci es
33
because that
method does not di sti ngui sh di vergent from uni form
sel ecti on (Box 1).
TRENDS in Ecology & Evolution Vol.16 No.7 J uly 2001
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375 Review
Table 1.Tests of ecological speciation in nature
Test Taxon
a
Result and implication: consistent (c) or inconsistent (i) with Ref s
ecological speciation
Rate of evolution of Hawaiian versus mainland Evolution of reproductive isolation is not faster in Hawaiian 34
reproductive isolation is Drosophilaspp. pairs Drosophilathan in mainland Drosophila (i)
correlated with strength Lake whitefish in different postglacial Gene flow is inversely correlated with level of morphological divergence (c) 35
of divergent selection lakes
Ecological selection Threespine sticklebacks in postglacial F1 hybrid growth rate is lower in the wild than in the lab; rank order of 15,
b
reduces hybrid fitness lakes growth rates of backcross hybrids reverses between parental habitats (c)
Darwins ground finches
1
F1 hybrid survival fluctuates with resource distribution (c) 45,46
Butterfly races F1, F2 and backcross hybrids have higher viability in the lab than 39
in the wild, and predation is major agent of selection (c)
Trait under divergent Threespine sticklebacks in postglacial Mating compatibility is influenced by body size and by nuptial 49,58
selection influences lakes coloration (c)
reproductive Monkey flowers
1
on different soils Postzygotic isolation is a pleiotropic effect of a gene encoding 47
compatibility tolerance of copper-contaminated soil (c)
Monkey flowers
2
Divergent selection by pollinators is detected on floral traits and 48
underlying quantitative trait loci (c)
Darwins ground finches
2
Beak and body size, under divergent selection, influence vocal 50,51
signals and are used as cues in interspecific mate discrimination (c)
Pea aphids on different host plants Divergent selection occurs on host-plant choice, which 41
determines premating isolation (c)
Host races of apple maggot fly on Divergent selection on diapause influences timing of emergence (c) 40,61
different host plants
Parallel evolution of Threespine sticklebacks in postglacial Independently evolved populations of the same ecotype show 55
mating incompatibilities lakes strong premating isolation, whereas populations of different
over similar ecotypes show little or no premating isolation (c)
environmental gradients Freshwater amphipod from two types Mating compatibility between populations is high when body size and 59
of environment environment type are similar, but is low when they are different (c)
Leaf beetles on different host plants Premating isolation is high between populations from same 60
host plants, but is low between those on different host plants (c)
a
Latin names: Apple maggot fly, Rhagoletis pomonella; Butterfly, Heliconius erato; Darwins ground finches, Geospiza fuliginosa
1
and G. fortis
1
, and Geospizaspp.
2
;
Freshwater amphipod, Hyalella azteca; Fruit flies, Drosophilaspp.; Lake whitefish, Coregonus spp.; Leaf beetles, Neochlamisus bebbianae; Monkey flowers
1
, Mimulus
guttatus; Monkey flowers
2
, Mimulus cardinalis and M. lewisii; Pea aphids, Acyrthosiphon pisum; Threespine sticklebacks, Gasterosteus spp.
b
H.D. Rundle, unpublished.
Divergent selection and the rate of evolution of
reproductive isolation
The study of ADAPTI VE RADI ATI ON suggests that
speci ati on rates are often el evated duri ng peri ods of
ecol ogi cal and phenotypi c di fferenti ati on
34
(see
Barracl ough and Nee
19
, thi s i ssue). Darwi ns fi nches
appear to exempl i fy thi s pattern (Fi g. 3): one
expl anati on i s that i f the l evel of phenotypi c
di fferenti ati on i s i ndi cati ve of strength of di vergent
sel ecti on, then reproducti ve i sol ati on evol ves most
qui ckl y when di vergent sel ecti on i s strongest. A
correl ati on between strength of di vergent sel ecti on
and rate of evol uti on of reproducti ve i sol ati on i s a
predi cti on of ecol ogi cal speci ati on (Tabl e 1).
The correl ati on between strength of di vergent
sel ecti on and rate of evol uti on of reproducti ve
i sol ati on has not been measured, probabl y because
di vergent sel ecti on i s di ffi cul t to quanti fy. I nstead,
researchers have used i ndi rect measures (Fi g. 3). Lu
and Bernatchez
35
compared gene fl ow wi th the l evel
of morphol ogi cal di fferenti ati on between I NCI PI ENT
SPECI ES of dwarf and normal l ake whi tefi sh Coregonus
i n several postgl aci al l akes of eastern Canada and
northern Mai ne (USA). Esti mated l evel s of gene fl ow
between sympatri c dwarf and normal popul ati ons
were l owest where morphol ogi cal di fferences between
the forms were greatest. Thi s i s consi stent wi th the
predi cti on of ecol ogi cal speci ati on i f the degree of
morphol ogi cal di fferenti ati on i s a good i ndex of
strength of di vergent sel ecti on. Al ternati vel y, the
strength of di vergent sel ecti on i s not di fferent
between l akes, and vari ati on i n morphol ogi cal
di fferenti ati on resul ts i nstead from vari ati on i n gene
fl ow. Prel i mi nary measurements of the resources
avai l abl e i n the l akes suggest that the strength of
di vergent sel ecti on i s di fferent between l akes
35
.
I n a second test of the predi cti on, I used Coyne and
Orr s
36,37
survey of Drosophilato compare the
strength of reproducti ve i sol ati on i n pai rs of
Hawai i an pi cture-wi nged Drosophilawi th the
strength of i sol ati on i n pai rs of popul ati ons and
speci es of conti nental Drosophilaof si mi l ar age
34
. The
Hawai i an Drosophilaare a di verse group havi ng a
hi gh speci ati on rate and possi bl y a hi gher overal l rate
of phenotypi c and ecol ogi cal di fferenti ati on. However,
no di fference was detected between Hawai i an and
conti nental Drosophilai n the average strength of
premati ng or postmati ng i sol ati on between si mi l ar-
aged popul ati ons, a resul t that does not support the
predi cti on of ecol ogi cal speci ati on. The rel i abi l i ty of
the test i s uncertai n, however, because nothi ng i s
known about the strength of di vergent sel ecti on i n
ei ther Hawai i an or conti nental Drosophila.
Ecological selection against hybrids
Stronger evi dence for ecol ogi cal speci ati on i s that
di vergent sel ecti on ari si ng from features of the
envi ronment di rectl y reduces fi tness of hybri ds (and
other i ndi vi dual s of i ntermedi ate phenotype) between
coexi sti ng speci es (ECOLOGI CAL MECHANI SM OF REDUCED
HYBRI D FI TNESS). Such postmati ng i sol ati on can ari se
because an i ntermedi ate phenotype i s l ess effi ci ent at
capturi ng prey i n the wi l d, or because i ntermedi ate
defenses l eave the hybri d suscepti bl e to predati on
and parasi ti sm. Thi s type of i sol ati on i s envi ronment
dependent and shoul d vani sh i n a common l aboratory
setti ng
4,38
. By contrast, geneti c mechani sms of
reduced hybri d fi tness ari se from I NTRI NSI C
I NCOMPATI BI LI TI ES between genes i nheri ted from the
parent speci es, and shoul d be mani fested i n every
envi ronment. Whereas geneti c mechani sms of
reduced hybri d fi tness coul d ari se duri ng ecol ogi cal
and non-ecol ogi cal speci ati on, di rect reducti on of
hybri d fi tness by ecol ogi cal sel ecti on pressures are a
uni que predi cti on of ecol ogi cal speci ati on (Box 1).
Demonstrati ons of ecol ogi cal sel ecti on agai nst
hybri ds are sti l l few (Tabl e 1 l i sts onl y the strongest
tests). F1 hybri ds between the l i mneti c and benthi c
speci es of threespi ne sti ckl ebacks have a hi gh fi tness
i n the l aboratory but an i ntermedi ate phenotype that
compromi ses thei r abi l i ty to acqui re food from the two
mai n habi tats i n thei r nati ve l akes. The resul t i s
sl ower growth of F1 hybri ds rel ati ve to ei ther parent
speci es when transpl anted to the habi tat of that
parent
15
. Furthermore, rel ati ve growth rates of
l i mneti c and benthi c backcrosses are reversed
between habi tats, as woul d be expected i f hybri d
fi tness i s di rectl y reduced by ecol ogi cal sel ecti on
pressures (H.D. Rundl e, unpubl i shed). A si mi l ar
pattern of hi gh vi abi l i ty of hybri d crosses i n the
l aboratory, coupl ed wi th reduced vi abi l i ty i n the wi l d,
i s seen i n crosses between two PARAPATRI C RACES of the
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Fig. 3. A phylogenetic
tree showing the possible
correlation between
ecological diversification
and speciation rate in the
Darwins finches
(Geospizaspp.). The high
diversity of beak traits
among species within the
CLADE of tree and ground
finches (outlined in red)
contrasts with the lower
diversity of beak traits
among species of the
three older LINEAGES.
Speciation rates are also
highly uneven, being
significantly greater in the
tree and ground finch
clade than in the rest of
the tree (P =0.011,
calculated using the
Nee et al.
62
equal-rates
test for multiple lineages).
Data are taken from Ref.
63. Bird images are
reproduced, with
permission, from
Ref. 65.
butterfl y Heliconius eratoi n Peru
39
. Sel ecti on agai nst
rare warni ng col or phenotypes i n nature by avi an
predators appears to be the cause.
Di fferences i n ti mi ng and durati on of di apause of
host races of the appl e maggot fl y Rhagoletis
pomonellarepresent adaptati ons to the ti mi ng of frui t
producti on of di fferent host pl ants i n rel ati on to the
ti mi ng of wi nter
40
. Hybri d offspri ng of i ndi vi dual s
that swi tch hosts shoul d be heavi l y di sadvantaged as
a consequence, al though thi s has not been
demonstrated di rectl y. Sel ecti on agai nst F1 hybri ds
between host races of pea aphi ds Acyrthosiphon
pisumon host pl ants of both parent speci es probabl y
has an ecol ogi cal basi s, but thi s has not yet been
confi rmed
41
. Crai g et al.
42
showed that F1 and F2
hybri ds between two host races of the fl y Eurosta
solidaginissurvi ved poorl y on the host pl ants of thei r
parents, al though the pattern of fi tnesses was
compl ex. An extended season of l eaf producti on by
hybri ds between popl ar Populusspp. mi ght expl ai n
the much hi gher l evel s of i nsect herbi vory that they
experi ence compared wi th those on the parent
speci es
43
. Reci procal transpl ants al ong an el evati on
gradi ent of two subspeci es of sagebrush Artemisia
tridentataand thei r hybri ds i ndi cated that each of the
three popul ati ons has hi ghest fi tness i n i ts own
envi ronment, wi th the hybri ds bei ng most fi t at an
i ntermedi ate el evati on
44
. Hybri ds i n the l ast two
studi es were nei ther F1 nor F2 hybri ds, but were
i ndi vi dual s from popul ati ons of hybri d ori gi n.
Ecol ogi cal l y based postmati ng i sol ati on i s
expected to change as envi ronments change. For
exampl e, Grant and Grant
45,46
recorded the fates of
i ndi vi dual hybri ds made of crosses between two
speci es of ground fi nch (Geospiza fuliginosaand G.
fortis) over 20 years on a Gal pagos i sl and. Hybri d
survi val was typi cal l y poor, owi ng to the l ow
abundance of seeds that the hybri ds coul d handl e
effi ci entl y. However, seed abundances were changed
si gni fi cantl y i n the years fol l owi ng a dramati c El Ni o
event i n whi ch rai nfal l i ncreased by an order of
magni tude. Remarkabl y, the greater rel ati ve
abundance of smal l seeds el i mi nated the di fference i n
survi val between hybri ds and the domi nant parent
speci es, G. fortis.
Ecological traits underlying reproductive isolation
Evi dence for ecol ogi cal speci ati on i s gai ned when
speci fi c genes or phenotypi c trai ts known to be under
di vergent sel ecti on between envi ronments are found
to be the basi s of reproducti ve i sol ati on (or are
geneti cal l y correl ated wi th trai ts that are the basi s of
reproducti ve i sol ati on) (Tabl e 1). For exampl e, i n the
monkey fl ower Mimulus guttatus, al l el es conferri ng
tol erance to soi l s contami nated wi th copper are
l ethal when combi ned i n the offspri ng of crosses wi th
pl ants from uncontami nated soi l s
47
. Reproducti ve
i sol ati on between two other monkey fl owers (M.
cardinalisand M. lewisii) i s associ ated wi th
di fferences i n fl oral trai ts that attract di fferent
pol l i nators and therefore contri bute to premati ng
i sol ati on. Mimulus lewisii has broad, fl at, pi nk petal s
wi th yel l ow nectar gui des, smal l nectar vol ume, and
i s pol l i nated pri mari l y by bumbl ebees, whereas M.
cardinalishas a narrow tubul ar corol l a and l arge
nectar rewards and i s pol l i nated pri mari l y by
hummi ngbi rds. These di vergent adaptati ons to
contrasti ng pol l i nators contri bute to premati ng
i sol ati on, and pol l i nators are attracted to arti fi ci al F2
hybri ds i n proporti on to the mi xture of genes from
the preferred parent
48
.
Body si ze i s strongl y di vergent between sympatri c
sti ckl eback speci es, and several l i nes of evi dence
suggest that thi s di fference i s the resul t of contrasti ng
natural sel ecti on between the mai n habi tats that they
expl oi t
49
. Body si ze was al so found to affect strongl y
the probabi l i ty of i nterspeci fi c hybri di zati on i n no-
choi ce l aboratory tri al s: crossbreedi ng occurred onl y
between the l argest i ndi vi dual s of the smal l est
speci es and the smal l est i ndi vi dual s of the l argest
speci es
49
. Si mi l arl y, i n Darwi ns fi nches, si ze and
shape of the beak and body, whi ch are strongl y
sel ected for effi ci ent expl oi tati on of di fferent foods,
are al so used as cues i n i nterspeci fi c mate
di scri mi nati on
50
. Some di vergence i n song, al bei t
i ncompl ete, mi ght accompany di vergence of si ze and
shape of the beak i n Darwi ns fi nches, and thi s coul d
al so i nfl uence premati ng i sol ati on
51
.
Adapti ve l i fe-hi story di fferenti ati on mi ght l ead to
reproducti ve i sol ati on i n many i nsects
52
. For exampl e,
di fferent ti mi ng of emergence between the appl e and
hawthorn races of the appl e maggot fl y i s l i nked to
changes i n the ti mi ng and durati on of di apause
40
.
Devel opment ti me i n popul ati ons of Drosophila
mojavensishas di verged between popul ati ons on
di fferent cactus hosts, and thi s trai t i s geneti cal l y
correl ated wi th behavi oral trai ts that i nfl uence
reproducti ve i sol ati on
53
.
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Different
(limnetic benthic)
Same
(limnetic limnetic
P
r
o
b
a
b
i
l
i
t
y

o
f

s
p
a
w
n
i
n
g

(
a
d
j
u
s
t
e
d
)
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
A B C D
Type of environment
benthic benthic)
Fig. 4. Parallel evolution
of premating isolation
between benthic and
limnetic threespine
sticklebacks
(Gasterosteus spp.) from
three lakes. Each circle
indicates frequency of
matings between males
and females from a pair of
populations, measured in
no-choice laboratory
mating trials. Pairs of
populations from the
same lake are indicated in
green; values in columnD
are mating frequencies
between males and
females from the same
population. Pairs of
populations from
different lakes are
indicated in blue. Pairs of
populations occurring in
the same type of
environment (Cand D)
mate with higher
frequency than do pairs
of populations from
different types of
environments (A and B).
Modified, with
permission, from Ref. 55.
Parallel speciation
Evi dence for ecol ogi cal speci ati on i s gai ned when
trai ts determi ni ng mati ng compati bi l i ty evol ve i n
paral l el i n di fferent popul ati ons experi enci ng si mi l ar
envi ronments (PARALLEL SPECI ATI ON
54,55
). Threespi ne
sti ckl ebacks provi de the cl earest case (Fi g. 4).
Sympatri c l i mneti c and benthi c speci es of threespi ne
sti ckl ebacks have ari sen i ndependentl y as many as
four ti mes i n separate l akes
56,57
. The two speci es
wi thi n a l ake rarel y (i f ever) hybri di ze i n the wi l d.
Frequency of hybri d mati ng i s rai sed to 1015% i n no-
choi ce l aboratory mati ng tri al s (Fi g. 4, col umn A),
whi ch i s si gni fi cantl y bel ow the val ue for mal es and
femal es from the same popul ati on (Fi g. 4, col umn D).
Remarkabl y, l i mneti cs and benthi cs from di fferent
l akes al so hybri di ze at l ow frequency i n the l aboratory
(Fi g. 4, col umn B), whereas popul ati ons of the same
ECOTYPE from di fferent l akes (i .e. both l i mneti c or both
benthi c) mate at hi gh frequency (Fi g. 4, col umn C).
Thi s pattern i mpl i es that trai ts i nfl uenci ng mati ng
compati bi l i ty have evol ved i n paral l el under si mi l ar
envi ronmental condi ti ons, strongl y i mpl i cati ng
di vergent natural sel ecti on i n the ori gi n of sti ckl eback
speci es
55
. Some nonecol ogi cal processes of speci ati on
mi ght al so yi el d paral l el evol uti on of mati ng
compati bi l i ty (e.g. pol ypl oi d speci ati on), but no
consi stent associ ati on between mati ng compati bi l i ty
and envi ronment i s expected. The trai ts determi ni ng
mati ng compati bi l i ty i n sti ckl ebacks are not known,
but body si ze
49
and nupti al col orati on
58
probabl y each
pl ay a rol e.
Freshwater amphi pods Hyalella aztecaoccur i n
two types of l akes. Lakes wi th predatory sunfi sh
contai n a smal l -bodi ed ecotype, whereas l akes l acki ng
fi sh predators contai n a l arge-bodi ed ecotype. Body
si ze di fferences between amphi pod popul ati ons are
geneti cal l y based and are not cl osel y correl ated wi th
el ectrophoreti c di stance
59
, suggesti ng that mul ti pl e
transi ti ons i n si ze have occurred. I ndi vi dual s from
popul ati ons of the same ecotype (i .e. both l arge or
both smal l ) readi l y i nterbreed, whereas i ndi vi dual s
from di fferent ecotypes do not
59
. Agai n, envi ronment
and phenotype predi ct mati ng compati bi l i ty better
than do geneti c rel ati onshi ps.
Funk
60
exami ned l evel s of premati ng i sol ati on
between popul ati ons of the l eaf beetl e Neochlamisus
bebbianae, a speci es that expl oi ts di fferent host
pl ants i n di fferent parts of i ts range. Mati ng tri al s
were carri ed out wi th two popul ati ons adapted to
mapl e Acer rubrum, one adapted to bi rch Betula
nigra, and one from wi l l ow Salix bebbiana. Leaves
from the host pl ants were present i n hal f the tri al s
and absent from the other hal f, but thi s made no
di fference to the resul ts. Reproducti ve i sol ati on was
strong between the bi rch popul ati on and both mapl e
popul ati ons, and between the wi l l ow popul ati on and
both mapl e popul ati ons (i sol ati on between wi l l ow and
bi rch popul ati ons was not tested), but was absent
between the two mapl e popul ati ons. However, geneti c
di vergence (based on mi tochondri al DNA) was
greater between the two mapl e popul ati ons than
between one of the mapl e popul ati ons and the wi l l ow
popul ati on, suggesti ng that reproducti ve i sol ati on i s
better predi cted by envi ronment than by PHYLOGENY.
Discussion
Speci ati on i s one of the l east understood major
features of evol uti on. The mai n obstacl e to progress i s
the vari ety of mechani sms that mi ght l ead to the
evol uti on of reproducti ve i sol ati on (Box 1), any one of
whi ch can be di ffi cul t to rul e out i n a speci fi c case. The
upshot i s that i t i s sti l l di ffi cul t to poi nt to even two
speci es i n nature and state wi th confi dence the
mechani sm that produced them. The excepti ons are
speci ati on events resul ti ng from pol ypl oi dy, because
pol ypl oi dy l eaves a cl ear geneti c si gnature for a
substanti al peri od of ti me. However, speci ati on by
pol ypl oi dy i s rel ati vel y common onl y i n pl ants, and,
even i n that taxon, probabl y accounts for onl y a
mi nori ty of speci ati on events
32
. The vast majori ty of
speci ati on events i n nature must therefore be
expl ai ned by other processes.
One of these other processes i s ecol ogi cal
speci ati on, dri ven by di vergent natural sel ecti on on
trai ts and resul ti ng from features of the envi ronment.
Ecol ogi cal speci ati on i s probabl y more easi l y tested
than i s speci ati on by geneti c dri ft or speci ati on
resul ti ng from the accumul ati on of al ternati ve
i ncompati bl e mutati ons under uni form sel ecti on.
Thi s i s because, si mi l ar to speci ati on by pol ypl oi dy,
di vergent natural sel ecti on often l eaves a si gnature i n
the pattern of reproducti ve i sol ati on, at l east for a
ti me (further geneti c di vergence after speci ati on i s
compl ete mi ght el i mi nate the si gnature). For
exampl e, whereas geneti c mechani sms of
reproducti ve i sol ati on are the expected outcome of
every speci ati on process (Box 1), ecol ogi cal l y based
sel ecti on agai nst hybri d phenotypes i s a uni que
predi cti on of ecol ogi cal speci ati on
15
(H.D. Rundl e,
unpubl i shed).
Si mi l arl y, paral l el speci ati on i s compel l i ng
evi dence that di vergent natural sel ecti on has
ul ti matel y brought about the evol uti on of
reproducti ve i sol ati on, as i s the fi ndi ng that trai ts
under di vergent natural sel ecti on are the basi s of
reproducti ve i sol ati on (or are geneti cal l y correl ated
wi th trai ts that form the basi s of reproducti ve
i sol ati on). A correl ati on between strength of di vergent
sel ecti on and the rate of evol uti on of reproducti ve
i sol ati on woul d be further evi dence of ecol ogi cal
speci ati on, but strength of di vergent sel ecti on i s not
easi l y measured. Fi nal l y, persi stence of ecol ogi cal l y
di fferenti ated popul ati ons i n the face of gene fl ow, and
evi dence of sympatri c speci ati on coupl ed wi th strong
ecol ogi cal di fferenti ati on, al so poi nt to ecol ogi cal
speci ati on (Vi a
8
, thi s i ssue), but al ternati ve
mechani sms can produce such patterns and must be
tested.
Recent progress has been made i n testi ng
ecol ogi cal speci ati on i n nature (Tabl e 1). Al though few
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i n number, candi date exampl es al ready i ndi cate the
mul ti pl e ways that di vergent sel ecti on mi ght l ead to
reproducti ve i sol ati on. For exampl e, at l east one
candi date for sympatri c speci ati on i s represented
(Rhagoletis), al though most speci es pai rs appear to
have hi stori es that i ncl ude an al l opatri c phase
(e.g. threespi ne sti ckl ebacks, Darwi ns ground fi nches
and Coregonus). The cases of ecol ogi cal speci ati on
i ncl ude popul ati ons and speci es whose hybri ds fai l
partl y because of i ntri nsi c geneti c i ncompati bi l i ti es
(e.g. Mimulus guttatusand Coregonus), and hybri ds
of other popul ati ons and speci es whose fi tness
depends on features of envi ronment (e.g. threespi ne
sti ckl ebacks; Darwi ns ground fi nches and Heliconius
erato). Evi dence for rei nforcement i s seen i n one case
(threespi ne sti ckl ebacks) but even i n thi s exampl e, as
i n others (Tabl e 1), consi derabl e reproducti ve
i sol ati on appears to have evol ved purel y as a by-
product of di vergent sel ecti on. Our understandi ng of
the range of processes i nvol ved i n ecol ogi cal
speci ati on wi l l i ncrease as more exampl es
accumul ate.
Neverthel ess, the evi dence for ecol ogi cal
speci ati on i s i ncompl ete. More tests from nature are
badl y needed, not onl y on the systems al ready
i denti fi ed as good candi dates (Tabl e 1) but al so i n
other systems. The general i ty of ecol ogi cal speci ati on
i s a l ong way from bei ng deci ded, but at l east there are
both tool s avai l abl e wi th whi ch to address the
probl em, and some promi si ng i ndi cati ons from a few
studi es of speci es i n the wi l d.
The mechani sms dri vi ng ecol ogi cal speci ati on al so
need to be more ful l y understood. What are the
ecol ogi cal agents of di vergent sel ecti on? How
i mportant are speci es i nteracti ons to strengtheni ng of
reproducti ve i sol ati on duri ng the sympatri c phase? I s
the by-product mechani sm effecti ve by i tsel f, and
responsi bl e for the bul k of the evol uti on of
reproducti ve i sol ati on i n al l opatry and sympatry, or
does rei nforcement i n sympatry pl ay a vi tal rol e i n the
fi nal producti on of two coexi sti ng speci es from a
si ngl e ancestor? I s di vergent sexual sel ecti on often
the outcome of di vergent natural sel ecti on, or does i t
ari se i ndependentl y from other processes?
The l i nk between ecol ogi cal speci ati on and
adapti ve radi ati on al so needs to be assessed
34
.
Di vergent natural sel ecti on i s an i mportant process i n
phenotypi c di fferenti ati on i n adapti ve radi ati on and,
for thi s reason, i t mi ght be expected to contri bute al so
to speci ati on, but thi s i s l ess wel l understood. I s
speci ati on i n adapti ve radi ati on chi efl y ecol ogi cal
speci ati on? How do the agents of di vergent sel ecti on,
the trai ts that are i ts targets, and the consequences
for reproducti ve i sol ati on, change as an adapti ve
radi ati on proceeds and the numbers of speci es i n the
envi ronment bui l ds? How durabl e are ecol ogi cal
speci es(the products of ecol ogi cal speci ati on): gi ven
the i mportance of ecol ogi cal context i n determi ni ng
hybri d fi tness, at l east when the speci es are young,
are ecol ogi cal speci es parti cul arl y prone to exti ncti on
when envi ronments change? I f so, how do the
mechani sms of speci es ori gi n affect the bui l d up of
speci es duri ng adapti ve radi ati on?
These questi ons emphasi ze the substanti al
chal l enges for research posed by Dobzhanskys
3
cl ai m,
one of the cl earest earl y statements of the hypothesi s
of ecol ogi cal speci ati on, that the genotype of a speci es
i s an i ntegrated system adapted to the ecol ogi cal
ni che i n whi ch the speci es l i ves. Gene recombi nati on
i n the offspri ng of speci es hybri ds may l ead to
formati on of di scordant gene patterns. Here,
Dobzhansky was referri ng to the bui l d up of geneti c
mechani sms of postmati ng i sol ati on, but the
hypothesi s i s general and appl i es equal l y wel l to
trai ts causi ng premati ng i sol ati on these too mi ght
be the product of adaptati on to envi ronments.
Happi l y, we are unl i kel y to have to wai t another 50
years before the chal l enge i s taken up, and the
hypothesi s recei ves the ful l eval uati on that i t
deserves.
TRENDS in Ecology & Evolution Vol.16 No.7 J uly 2001
http://tree.trends.com
379 Review
Acknowledgements
I thank N. Barton, S. Via
and other anonymous
reviewers for their
suggestions. My research
is funded by the Natural
Sciences and Engineering
Research Council of
Canada (NSERC).
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