Eberhard M.J. 1986 Alternative Adaptation, Speciation And
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Proc. Nati. Acad. Sci. U S A Vol. 8 3, p p . 1388-1392, March 1986 Evolution Alternative adaptations, speciation, a n d phylogeny ( A Review) (polymorphism/epigenetlc plasticity/macroevolutlon/punctuated equilibria/regulatory evolution) MARY JANE WEST-EBERHARD* Smithsonian Tropical Research Institute, Balboa, Panama Communicated b y Charles D. Michener, October 1 5, 1985 ABSTRACT Alternative adaptations-different adaptive phenotypes maintained i n t h e same life stage a n d t he same population b u t n o t necessarily simultaneouslyexpressed i n t h e same individual-represent contrasting character sets pro- ducedby t h e same genome, i n effect allowing a single species t o occupy more than o n e sympatric niche. Such alternatives a r e particularly likely t o give rise t o novel adaptations because o f selection f o r extreme dissimilarity between them a n d because established traits buffer populations against extinction while independentlyexpressed alternatives evolve i n n e w directions. Particular alternatives ca n b e suddenly fixed i n populations with little o r n o genetic change, leading t o a period ofrapid evolution (especially, o f morphology) exaggerating t h e charac- teristics o f t h e newly fixed form. This burst o f change would facilitate rapid speciation a n d could produce "punctuated" patterns o f evolution. Evidence from a wide variety o f orga- nisms shows that alternative phenotypes ar e exceedingly com- m o n i n nature a n d that they ar e probably important i n speciation a n d macroevolution. Although many o f these ideas a n d observations have been piecemeal b y previous authors, bringing them together demonstrates t h e probable importance o f alternative adaptations i n t h e origin o f major evolutionary novelties a n d calls f o r a revision of current a n d traditional ideas about t he role o f behavior a n d ontogeny i n t h e genesis o f organic diversity. T h e Alternative-Adaptation Hypothesis T h e purpose o f this paper i s t o suggest a change i n t h e w a y biologists think about t h e origins o f organic diversity: char- acter divergence, speciation, a n d macroevolution o r t h e invasion o f major n ew adaptive zones. T h e usual w a y t o visualize phylogenetically important divergence begins with reproductive isolation, o r speciation: a branching point o f a phylogenetic tree marks both t h e beginning o f a ne w lineage a n d t h e beginning o f character divergence. N e w characters may conceivably arise without reproductive isolation v i a gradual evolution over time, with t h e eventual formation o f a new "chronospecies". B u t increased diversity a n d major innovation begin with speciation, a n d macroevolution leading t o t h e origin of a n w higher taxon requires a series o f such events. O n this evolutionists have generally agreed, even when holding otherwise disparate opinions (e.g., s e e p . 524 o f ref. 1, p . 171 o f ref. 2, a n d p . 1 7 4 o f ref. 3 and, f o r a n exception, ref. 4 ) . I propose a very different view o f divergence a n d phylogeny. I n this "alternative adaptation" hypothesis, nov- e l traits originate a n d become elaborated as stable alternative phenotypes o r morphs within species, prior t o reproductive isolation a n d speciation, when they come t o characterize distinctive n e w lineages. That i s , drastic innovation c a n begin n o t with t h e branching of a phylogenetic tree but with t h e bifurcation o f a developmental o r behavioral program ("epigenetic divergence") giving rise to intraspecific alter- native adaptations. 1388 Alternative adaptations a r e different, often complex, evolved phenotypes occurring i n t he same lifestage a n d th e same population b u t n o t necessarily simultaneously e x- pressed i n t h e same individual. [When "adaptation" sensu Williams (5 ) i s n o t applicable o r intended I will u s e t h e more general words "phenotype" o r "form."] Examples ar e familiar t o everyone. They include t h e "workers" a n d "queens" o f social insects (6); males a n d females o f sexually reproducing species; a n d t he contrasting morphs o f batesian mimics i n butterflies (7). T he particular phenotype expressed i n a given individual o r a t a given time depends on t h e state o f a regulatory ("switch") mechanism, which c an b e either condition-sensitive o r genetic (allelic, chromosomal, o r a supergene), producing "facultative" a n d "genetic-switch" alternatives, respectively (7-10). For purposes o f t h e present argument i t matters little which type o f switch mechanism i s involved; i n both cases t he phenotypes themselves ar e ''genetic" i n that they involve t h e coordinated expression o f differentsuites of genes (different coadaptivegene sets); and, with t h e exception of t h e relatively small number of genes involved i n a genetic-switch mechanism, the genes required f o r t h e production of both or a l l alternative phenotypes a r e borne b y a l l individuals i n t he population. I n brief outline, evolution i n accord with t h e "alternative adaptation" hypothesis proceeds a s follows: A s e t o f alter- native phenotypes becomes established a s a stable feature o f a population, an d is gradually improved by selection, possi- b l y leading t o a "macroevolutionary" degree of distinctive- ness between alternatives. Then conditions (e.g., i n a geo- graphically isolated population) m y favor only o n e of t h e alternatives, leading t o i t s exclusive expression with little o r n o genetic change. This m ay b e accompanied b y rapid evolution as t h e genome i s released from t he constraints o f having to accommodate multiple alternatives. This could facilitate speciation b y accentuating divergence from t h e parent population, producing a n e w lineage characterized b y t he newly fixed n d no w modified form. These occurrences a r e further discussed below, along with examples from a variety o f organisms. Evolutionary Properties of Alternative Adaptations Alternative phenotypes a r e a kind of "covariant character set" (8). Others include hormonally regulated sets o f male a n d female traits, functionally an d morphologically differen- tiated larval a n d adult characters, a n d even t h e contrasting tissue a n d organ systems o f a multicellular individual. I n al l of these cases t h e coordinated expression o f a n underlying s e t o f genes i s governed b y switch mechanisms. T h e developmental significance o f a switch mechanism i s that i t determines that o n e s e t o f genes shall b e expressed instead o f another, alternative, set. T h e evolutionary significance o f a switch i s that i t determines which o f a n array o f potential phenotypes will b e expressed and, therefore, exposed t o *Address f o r correspondence: Escuela d e Biologia, Universidad de Costa Rica, Ciudad Universitaria, Costa Rica.
Eberhard M.J. 1986 Alternative Adaptation, Speciation And
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