Microevolution Rate, Pattern, Process

539 Pages·2002·17.65 MB·English

by  A. P. Hendry, M. T. Kinnison (auth.), A. P. Hendry, M. T. Kinnison (eds.)

MICROEVOLUTION: RATE, PATTERN, PROCESS
Contemporary Issues in Genetics and Evolution
VOLUME 8
The titles published in this series are listed at the end of this volume.
Microevolution
Rate, Pattern, Process
Edited by
A.P. HENDRY and M.T. KINNISON
Reprinted from Genetica, Volumes 112-113,2001
KLUWER ACADEMIC PUBLISHERS
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Contents
An introduction to microevolution: rate, pattern, process 1
A.P. Hendry, M.T. Kinnison
Theoretical developments and statistical methods
The adaptive landscape as a conceptual bridge between micro- and macroevolution 9
S.J. Arnold, M.E. Pfrender, A.G. Jones
Possible consequences of genes of major effect: transient changes in the G-matrix 33
A.F. Agrawal, E.D. Brodie III, L.H. Rieseberg
Toward a new synthesis: population genetics and evolutionary developmental 45
biology
N.A. Johnson, A.H. Porter
Epistasis, complex traits, and mapping genes 59
M.J. Wade
Population structure inhibits evolutionary diversification under competition for re 71
sources
T. Day
Variation, selection and evolution of function-valued traits 87
J.G. Kingsolver, R. Gomulkiewicz, P.A. Carter
Why the null matters: statistical tests, random walks and evolution 105
H.D. Sheets, C.E. Mitchell
Synthetic reviews and perspectives
Rates of evolution on the time scale of the evolutionary process 127
P.D. Gingerich
The pace of modern life II: from rates of contemporary microevolution to pattern and 145
process
M.T. Kinnison, A.P. Hendry
Trends and rates of microevolution in plants 165
E. Bone, A. Farres
The population ecology of contemporary adaptations: what empirical studies reveal 183
about the conditions that promote adaptive evolution
D.N. Reznick, c.K. Ghalambor
Explaining stasis: microevolutionary studies in natural populations 199
J. MeriHi, B.C. Sheldon, L.E.B. Kruuk
Ring species as bridges between microevolution and speciation 223
D.E. Irwin, J.H. Irwin, T.D. Price
Microevolution in island rodents 245
O.R.W. Pergams, M.Y. Ashley
Empirical demonstrations in natural systems
Genetic architecture of adaptive differentiation in evolving host races of the soapberry 257
bug, ladera haematoloma
S.P. Carroll, H. Dingle, T.R Famula, C.W. Fox
Rapid evolution of wing size clines in Drosophila subobscura 273
G.W. Gilchrist, RB. Huey, L. Serra
Insecticide resistance in the mosquito Culex pipiens: what have we learned about 287
adaptation?
M. Raymond, C. Berticat, M. Weill, N. Pasteur, C. Chevillon
High gene flow levels lead to gamete wastage in a desert spider system 297
S.E. Riechert, F.D. Singer, T.C. Jones
Integrating genetic and environmental forces that shape the evolution of geographic 321
variation in a marine snail
G.c. Trussell, RJ. Etter
On morphological clocks and paleophylogeography: towards a timescale for Sorex 339
hybrid zones
P.D. Polly
A population founded by a single pair of individuals: establishment, expansion, and 359
evolution
P.R Grant, B.R Grant, K Petren
Refugial isolation versus ecological gradients 383
T.B. Smith, CJ. Schneider, K Holder
Experimental studies of adaptive differentiation in Bahamian Anolis lizards 399
J.B. Losos, T.W. Schoener, KI. Warheit, D. Creer
Runaway social games, genetic cycles driven by alternative male and female 417
strategies, and the origin of morphs
B. Sinervo
Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in 435
cichlid fish
R Lande, O. Seehausen, J.J.M. van Alphen
Lateral plate evolution in the threespine stickleback: getting nowhere fast 445
M.A. Bell
Sexual conflict and evolution in Trinidadian guppies 463
A.E. Magurran
A century of life-history evolution in grayling 475
T.O. Haugen, L.A. V~llestad
Evolution of chinook salmon (Oncorhynchus tshawytscha) populations in New 493
Zealand: pattern, rate, and process
T.P. Quinn, M.T. Kinnison, MJ. Unwin
Adaptive divergence and the evolution of reproductive isolation in the wild: an empir- 515
ical demonstration using introduced sockeye salmon
A.P. Hendry
Genetica 112·113: 1-8,200l. 1
© 2001 Kluwer Academic Publishers. Printed in the Netherlands.
An introduction to microevolution: rate, pattern, process
A.P. Hendry! & M.T. Kinnison2
1 Organismic and Evolutionary Biology Program, University of Massachusetts, Amherst, MA 01003·5810, USA
(Phone: 413·577·2314; Fax: 413·545·3243; E·mail: [email protected]); 2Department of Biological
Sciences, Murray Hall, University of Maine, Orono, ME 04469·5751, USA (Phone: 207·581·2540; Fax:
207·581·2537; E·mail: [email protected])
Key words: adaptation, adaptive radiation, contingency, determinism, evolutionary rates, macroevolution,
microevolution, natural selection, speciation
Abstract
This special issue of Genetica brings together a diverse collection of contributions that examine evolution within
and among populations (i.e., microevolution), and the role that microevolution plays in the formation of new
species and morphological forms (i.e., macroevolution). Many of the papers present evidence of microevolution
occurring over contemporary time frames, further validating the near ubiquity of ongoing evolution in the world
around us. Several synthetic reviews of empirical work help to define the conditions under which microevolution
is or is not likely to occur. Some of the studies speak directly to current controversies in evolutionary biology, such
as the relative roles of determinism and contingency, and the nature of the relationship between microevolution
and macroevolution. In general, microevolution seems driven largely by deterministic mechanisms, particularly
natural selection, but contingency plays a role in (1) determining whether or not suitable conditions are present
for evolution to proceed, and (2) guiding the precise manner by which evolution proceeds. Several theoretical
treatments and empirical reviews confirm previous research in showing that microevolutionary processes are at
least capable of generating macroevolutionary trends. Macroevolution may indeed reflect microevolution writ
large but the pattern by which it arises is perhaps best characterized as microevolution writ in fits and starts.
Introduction with the evolution of higher systematic groups (mac
roevolution), which has long been of central interest.
Evolution is often considered in two categories: micro This serves to underline the above-cited consideration
evolution and macroevolution. The former obviously of the absence of any intrinsic connection between
implies a small amount of change and the later a large genetics and the doctrine of evolution, which deals
amount. The difficulty comes in deciding where the particularly with macroevolution' (from Filipchenko,
boundary between the two should fall, whether or not 1927, p. 93-94, translated by P. Gingerich, pers.
they reflect the same processes (acting over different comm.). In contrast, Dobzhansky (1937, p. 12) felt
time scales), and whether or not the dichotomy is even that the micro and macro of evolution were insepar
useful or valid. The collection of papers in this special able: 'Experience seems to show, however, that there
issue of Genetica is titled 'Microevolution: rate, pat is no way toward an understanding of the mechanisms
tern, process', which begs the question of just what is of macro-evolutionary changes, which require time on
meant by the term microevolution. A brief historical a geological scale, other than through a full compre
survey provides some perspective. hension of the micro-evolutionary process observable
The terms appear to have been coined by within the span of a human lifetime .. .'. The oppos
Filipchenko (1927, 1929): 'Modem genetics doubt ing argument, that for different mechanisms at the
less represents the veil of the evolution of Jordanian different scales of evolution, was continued most en
and Linnaean biotypes (microevolution), contrasted thusiastically by Goldschmidt (1940, p. 8), for whom
2
macroevolution was ' ... evolution of the good species logy, evolution, and conservation. This special issue
and all the higher taxonomic categories'. Mayr (1942, of Genetica is intended to provide a timely synthesis
p. 291) described the difference thus: 'Under the term of current information, an illustration of exciting new
microevolution such evolutionary processes are un directions, and a springboard for future investigations.
derstood as occur within short spaces of time and in We invited active evolutionary biologists to con
lower systematic categories, in general within the spe tribute theoretical developments and statistical meth
cies .... By the term macroevolution we understand the ods, synthetic reviews and perspectives, and empirical
development of new organic systems - in short, evolu demonstrations in natural systems. The resulting pa
tionary processes that require long periods of time and pers are concerned to varying degrees with the rate
concern the higher systematic categories .. .' . at which microevolution proceeds (rate), variation in
In Simpson's (1944, p. 97) opinion, 'Microe evolution over space and time (pattern), and mechan
volution involves mainly changes within potentially isms causing evolutionary change (process). Several
continuous populations, and there is little doubt that major themes emerged: descriptions of microevolution
its materials are those revealed by genetic experiment within and among populations, evidence for contin
ation. Macro-evolution involves the rise and diver gency versus determinism in microevolution, consid
gence of discontinuous groups, and it is still debatable erations of how microevolution contributes to mac
whether it differs in kind or only degree from micro roevolution, and the development and assessment of
evolution'. Simpson (1944) also pointed out that the theoretical models and statistical methods.
use of macroevolution by some biologists (species
level and above) was different from that adopted by
others (higher taxonomic levels). He suggested that Microevolution
the latter might more appropriately be called 'mega
evolution' (Simpson, 1944, p. 98), but later asserted It now seems almost quaint that microevolution was
' ... that all three of these somewhat monstrous termin ever seriously questioned as a prevalent and important
ological innovations have served whatever purpose phenomenon. At present, evolutionary biologists have
they may have had and that clarity might now be im illuminated so many concrete examples of evolution
proved by abandoning them' (Simpson, 1953, p. 339). ary change within populations that even the staunchest
Rensch (1954) was also critical of the terms, prefer critics tend to concede the reality of microevo1ution.
ring 'infraspecific' and 'transspecific'. Despite their Classic demonstrations include industrial melanism in
monstrosity, microevolution and macroevolution per peppered moths (Kettlewell, 1973; Majerus, 1998),
sist in the lexicon of biology. Indeed, they are dis adaptation of plants to different soil conditions (Snay
cussed in every major textbook on evolution (although don, 1970; Antonovics, Bradshaw & Turner, 1971),
definitions vary). divergence of mosquitofish introduced to Hawaii (Ste
For the purposes ofthis special issue, microevolu ams, 1983a,b), adaptation of guppies to different
tion refers to changes within and among populations. predation regimes in Trinidad (Endler, 1980; Reznick
Also considered are the formation and divergence of et aI., 1997), evolution of resistance to pesticides (Ta
new species by processes known to act within and bashnik, 1994) and antibiotics (Baquero & Blazquez,
among populations (e.g., natural and sexual selection, 1997), and changes in the size and shape of finch beaks
micromutation, genetic drift, gene flow). Defined in in the Galapagos Islands (Grant & Grant, 1995).
this way, microevolution is conceptually independent Model systems for investigating microevolution
of time scale, and so it is also useful to distinguish continue to be developed. This special issue includes
between contemporary microevolution (over one gen research in several such systems, including soapberry
eration to a few centuries) and microevolution occur bugs on introduced host plants (Carroll et aI., 2001),
ring over longer intervals (evident in paleontological Drosophila subobscura introduced to North America
series). In the past few decades, studies of microe (Gilchrist, Huey & Serra, 2001), mosquitoes adapting
volution have taken the legacy of the evolutionary syn to pesticides (Raymond et aI., 2001), riparian and arid
thesis to new levels of refinement, and now represent land spiders (Riechert, Singer & Jones, 2001), marine
the flagship for the presence and power of evolution. snails exposed to an introduced predator (Trussell &
This expanding interest has come with the develop Etter, 2001), European shrews (Polly, 2001), Darwin's
ment of new techniques (see below) and the realization finches (Grant, Grant & Petren, 2001), rainforest ver
of microevolution's relevance to many issues in eco- tebrates (Smith, Schneider & Holder, 2001), Anolis
3
lizards introduced to Bahamian Islands (Losos et aI., selection without any net change in the expected dir
2001), side-blotched lizards (Sinervo, 2001), African ection. They argue that this paradox may be explained
cichlids (Lande, Seehausen & van Alphen, 2001), by biased estimates of heritability, varying selection
threespine stickleback (Bell, 2001), Trinidadian gup in time or space, selection on environmental devi
pies (Magurran, 2001), grayling introduced to new ations, selection on correlated traits, or low statistical
sites in Norway (Haugen & V!1lllestad, 2001), chinook power. Furthermore, microevolution may go undetec
salmon introduced to New Zealand (Quinn, Kinnison ted with traditional approaches if changes taking place
& Unwin, 2001), and sockeye salmon introduced to at the genetic level are counteracted by simultan
Lake Washington (Hendry, 2001). eous and opposing environmental influences (see also
One benefit of multiple systems is that the data can Conover & Schlutz, 1995; Merila, Kruuk & Sheldon,
be combined into reviews that address general ques 2001).
tions about evolution. Examples include analyses of The above papers demonstrate that microevolu
heritability (Mousseau & Roff, 1987), genetic vari tion is a frequent phenomenon in nature, particularly
ance (Houle, 1992), and natural selection (Endler, when populations are exposed to new conditions. In
1986; Kingsolver et aI., 2001). Several papers in general, altered selection pressures lead to adaptive
the present volume provide reviews and syntheses of changes, many of which have a genetic basis. Adapt
contemporary microevolution. Pergams and Ashley ive microevolution may also be influenced by pheno
(2001) perform a meta-analysis on morphological data typic plasticity (Losos et aI., 2001; Trussell & Etter,
over the last century in four widely-separated island 2001). In contrast, microevolution appears to be con
rodent populations. They conclude that the observed strained in some situations, either because investigat
changes are best explained by natural selection, and ors cannot correctly measure the relevant parameters
that rates of evolution are higher on smaller and more or because specific conditions hamper adaptive diver
remote islands. Bone and Farres (2001) review rates gence. The reported instances of little or no adaptive
of microevolution in plants, concluding that evolution change within populations are not in conflict with neo
can be sustained under artificial selection but slows Darwinian theory because stasis or maladaptation can
with time in natural populations, and that physiolo be explained by selection, micromutation, gene flow,
gical traits evolve more rapidly than morphological and genetic drift (see also Barton & Partridge, 2000).
traits. Kinnison and Hendry (2001) build on Hendry
and Kinnison's (1999) earlier review of rates of con
temporary microevolution in animals. We find that Contingency versus determinism
natural selection is strong enough to explain observe
microevolution but that selection is probably rarely Are patterns of evolutionary diversification repeat
sustained over many generations, that life history traits able? The remarkable convergence of independent
evolve as fast as (or faster than) morphological traits, faunas into similar sets of niches on different con
and that evolutionary diversification increases with tinents or islands provides a classic argument for the
time but at a decreasing rate. deterministic nature of evolution (i.e., similar selective
What conditions favor adaptation and what condi pressures lead to similar adaptive solutions; Simpson,
tions do not? Reznick and Ghalambor (2001) review 1944, 1953; Lack, 1947; Schluter, 2000). Conversely,
studies of contemporary microevolution and conclude based on the 'Cambrian Explosion' and the Burgess
that a general condition favoring adaptive evolution is Shale fauna, Gould (1989) argued that contingency
colonization followed by an opportunity for popula (chance events) is so important that if the 'tape of
tion growth. Colonization opportunities may incl\lde life' were replayed, a similar outcome would be un
novel host or food resources, new biophysical environ likely. This conclusion has been disputed by one of the
ments, new predator communities, or human-modified prominent Burgess Shale researchers (Conway Mor
environments. The opportunity for population expan ris, 1998). Unfortunately, the Cambrian Explosion
sion is important because it reduces the probability and other such historical events are not replicated,
of extinction before adaptation is successful (see also leaving them of limited use in dissecting the relative
Gomulkiewicz & Holt, 1995). MeriHi, Sheldon and roles of contingency versus determinism. Such is not
Kruuk (2001), however, point out that when nat the case with microevolution, where independently
ural populations are monitored for extended periods, derived replicate populations are often exposed to
they often appear to be under sustained directional similar environmental conditions.
4
Microevolutionary studies reveal that similar se sticklebacks) and the manner by which adaptation
lective pressures acting on replicate populations tend proceeds (e.g., proximate or distal wing segment in
to result in remarkably convergent (from different Drosophila). The role of contingency in determining
starting conditions) or parallel (from similar starting the course of evolution presumably increases when the
conditions) adaptations. In guppies, for example, nu starting populations are more divergent (phylogenetic
merous low-predation populations have evolved sim constraints become increasing important) or smaller
ilar characteristics despite being derived independ (founder effects become increasingly important). The
ently from different high-predation populations (End role of contingency may also decrease with time along
ler, 1980, 1995; Reznick et aI., 1997). In Anolis a temporal sequence of adaptation. Determinism and
lizards, similar sets of ecologically-specialized forms contingency also influence the evolution of reproduct
have evolved independently from different ancestral ive isolation and may thus contribute to macroevolu
forms on multiple islands (Losos et aI., 1998; Losos tion. In sticklebacks, benthic females prefer to mate
et aI., 2001). In threespine stickleback, independent with benthic males and limnetic females with lim
freshwater populations have predictably evolved fewer netic males regardless of their lake of origin, providing
lateral plates than their marine or anadromous ancest strong evidence that parallel evolution in response
ors (Bell, 2001). In sockeye salmon, similar beach to natural selection has lead to 'parallel speciation'
and stream ecotypes have evolved independently in (Rundle et aI., 2000). In greenish warblers, how
many different lake systems (Hendry et aI., 2000; ever, parallel evolution of increased song complexity
Hendry, 2001). In chinook salmon introduced to New has initiated reproductive isolation because changes
Zealand, juvenile life history and reproductive invest in song complexity along different geographical paths
ment have evolved in response to growth conditions were caused by different modifications to song struc
and migration distance, respectively, in patterns re ture (Irwin, Bensch & Price, 2001; Irwin, Irwin &
markably similar to those observed within the species' Price, 2001).
native range (Kinnison et aI., 2001; Quinn et aI.,
2001).
Nested within the overall deterministic nature of Micro to macro
microevolution is an element of unpredictable con
tingency that can cause adaptation to vary in in Are macroevolutionary events (large morphological
teresting ways. In threespine stickleback, sympatric changes or speciation) simply the cumulative outcome
benthic and limnetic pairs have evolved in only six of microevolutionary mechanisms (micromutation, se
geographically-proximate lakes, suggesting specific lection, gene flow, genetic drift), or does macroevolu
geological conditions are necessary for their diver tion require some qualitatively different mechanism?
gence (i.e., 'double invasions', Taylor & McPhail, The history of this debate is long, convoluted, and
2000). In Drosophila subobscura, lattitudinal clines sometimes acrimonious. Many of the disagreements
in wing size have evolved independently in both nat before the evolutionary synthesis, such as the battle
ive and introduced popUlations but the particular wing between Biometricians and Mendelians, ultimately
segment causing the cline can vary (Huey et al., proved illusory (Provine, 1971). Accordingly, archi
2000; Gilchrist, Huey & Serra, 2001). In greenish tects of the evolutionary synthesis favored the equival
warblers, parallel increases in song complexity to the ency of micro and macro (Fisher, 1930; Dobzhansky,
north around the Tibetan plateau have been achieved 1937; Huxley, 1942; Mayr, 1942; Simpson, 1944,
through divergent changes in song structure (Irwin, 1953), although some contemporaries disagreed (e.g.,
Bensch & Price, 2001; Irwin, Irwin & Price, 2001). In Goldschmidt, 1940). Elements of the debate have
mosquitoes, resistance to pesticides frequently evolves changed to the present but differences of opinion
but the specific genes responsible may vary, at least remain strong.
early in the process of adaptation (Raymond et aI., For example, the history of life as recorded in
2001). the fossil record tends toward long periods of relat
It thus seems that microevolution is often driven ive stasis interrupted by short bursts of diversifica
by deterministic mechanisms, particularly natural se tion, with the geologically-instantaneous appearance
lection, but that contingency can play a role in de of new species. Some biologists have argued that this
termining whether or not suitable conditions present pattern conflicts with neo-Darwinian theory (Gould &
themselves (e.g., double invasions of freshwater by Eldredge, 1977; Stanley, 1979; Bennett, 1997 but see