- Email: [email protected]
Evolution of correlated characters
TREE vol.
7, no. 9, September
1992
( I’-19 I) Evol. Trends Plants 5, 109-I 23 28 Rothera, S.L. and Davy, A.I. (I 986) New Phytol. 102, 449-467 29 Brammal, R.A. and Semple, I.C. ( 19901 Can. I. BoT. 68, 2065-2069 30 Van Dijk, P., Hartog, M. and Van Delden, W. Biol /. Linn. Sot. (in press) 31 Stebbins, G.L. (19851 Ann. MO. Bat. Card. 72,824-832 32 Roose, M.L. and Cottlieb, L.D. (1976) E\,o/otion 30, 8 18-830 33 Shore, I.S. (1991) Heredity66, 305-321 34 Krebs, S.L. and Hancock, J.F. (1989) Heredity63, I I-18 35 Soltis, D.E. and Rieseberg, L.H. (19861 Am. /. Bat. 73, 3 I O-3 I8 36 Novak, S.I., Soltis, D.E. and Soltis, P.S. ( I 39 I ) Am. /. Bot. 78, 1586-l 600 37 Samuel, R., Pinsker, W. and Ehrendorfer,
F. ( I9901 Heredity 65, 369-378 38 Tomekpe, K. and Lumaret, R. (1991) Evolution 45,359-370 39 Thompson, I.D.. McNeilly, T. and Gray, 117, 141-152 A.j. (1991) NewPhytol. 40 Thompson, I.D. ( I99 I) Bioscience
4 I,
393-40 I 41 Macdonald,
S.E., Chinnappa, C.C. and Reid, D.M. (1988) Evolution 42, 1036-1046 42 Garbutt, K. and Bazzaz. F.A. (1983) New Phytol. 93, 129-l 41 43 Bever, I.D. and Felber, F. Oxf Sorv Evol. Biol. (in press) 44 McElroy, A.R. (1991) Euphytica 55, 117-123 45 Quarin, C.L. and Hanna, W.W ( 1980) Crop Sci. 20, 69-75 46 Marks, G.E (1966) Evolution 20, 552-557 47 Barrett, S.C.H. (19891 in Speciation and
Evolution
its Consequences (Otte, D. and Endler, J.A., eds), pp. 257-283, Sinauer 48 Ganders, F.R. (1989) in Genetics, Speciation and the Founder Principle (Giddings, L.V., Kaneshiro, K.Y. and Anderson, W.W., eds), pp. 99-l 12, Oxford University Press 49 Marshall, D.R. and Brown, A.H.D. (1981) Heredity32. 321-323 50 Normann, G.A. and Quarin, C.L. (1987) Cenome 29,340-344 M.D. (1991) 51 Wetth, C.R. and Windham. Am. Nat. I37,5 15-526 52 Pernes, 1. ( 1984) Gestion des Ressources CCnPtiques des Plantes, Tome 2: Manuel, Lavoisier 53 Endler, 1.A. (1989) in Speciation and its Consequences (Otte, D. and Endler, ].A., eds), pp. 625-648, Sinauer
of Correlated
Characters
Trevor Price and Tom Langen Muny traits are genetically correlated with each other. fius, selection that changes the mean value of one trait causes other traits to change as well. Recent comparative studies have emphasized the pxsible importance of such correlated rc!sponses in affecting the evolution of traits, including some Gehviors, which are of little adaptive significance, or even maladaptive. However, it is also possible for traits with major effects on fitness, srrch as brain size, to evolve entirely 6y r,?rrelated response. Other traits that do riot appear to have evolved at all may IIave been subject to much directional selection, simply to prevent their evolil tion by correlated response. The new i qterest in correlated responses reflects rqore rigorous attempts to consider the crganism as a whole, rather than dissectieg it into a num6er of questionably sepI:lrable traits. There are two main ways by which characters of no adaptive Ggnificance can evolve: genetic drift, and the correlated response IO selection on other characters. Correlated responses arise through pleiotropy (the multiple effects of individual genes) and linkage disequilibrium (nonrandom associ&ion between alleles at different :oci). Pleiotropy, in particular, is ‘Nidespread’, so correlated re~;ponses should be common. rrevor Price and Tom Langen are at the Dept of 3iology, 01 16, University of California at San Diego, _a lolla, CA 92093, USA. B 1992, Elsev~er Science Publishers
Ltd (UK)
Indeed, Sewall Wright’, who is perhaps better known for his theories involving genetic drift, thought that nonadaptive character differences among species (if they occur at all) are mostly attributable to pleiotropy and correlated response. The idea of correlated response is not new, being found in the earliest known coherent formulation of natural selection (see Ref. 2). It was discussed extensively by Darwir?, and is still regularly considered in discussions of neutral evolution, and in criticisms of pan-selectionism4-7. Correlated response has recently been discussed in two main contexts: the evolution of brainbody allometric patternPa, and the evolution of several different kinds of behaviors”-‘4. Each has engendered much controversy. Here, we review correlated response and discuss the way in which it relates to common ideas of adaptive evolution. We make three points. All have been made before, but each has also been overlooked in some recent discussions. First, a character whose interspecific variation is thought to be of major adaptive significance based on comparative or functional studies (e.g. relative brain size) may have evolved from some ancestral state entirely by
correlated response - evolution by correlated response does not necessarily imply neutrality. Secondly, characters that show no variation among species may nonetheless have been subject to much directional selection, otherwise they would have evolved as a consequence of genetic correlations with other characters that do differ among the species. In such cases, special reasons are needed to explain why these traits have not evolved. Thirdly, genetic correlations can greatly slow the evolution of weakly selected characters toward their optima15, and traits that are of little adaptive significance, or even strongly maladaptive, can persist indefinitely as a result of selection on other correlated traits. Identifying correlated responses The basic concept of correlated response can be illustrated with a simple genetic model (Box I ). When selection is applied to a single character, X, in some ancestral population, a second character, Y, evolves along a slope given by the additive genetic regression of Y on X (Fig. I). When selection is applied to Y but not X the population evolves along a slope given by the additive regression of X on Y. Any deviation from these 307
TREE vol. 7, no. 9, September
1992
Box 1. Correlate The
essenti
response can I plified modal 0J ation, adapted 1
below illustrate9/ characters, X d character is ei by many gen&a Assume that th genes: ‘A’ gene&:. pleiotropic) whc affect either X &%F.J there are equal class and all a same. Selection X by 1 unit leadi
due to A genes genes by 0.5 uni B genes onfy A?
slopes implies that both characters have been subject to some directional selection, given several assumptions (see below). The minimum amount of selection on each character can be determined using the method of LandeB I6 (Box 2). The method can compare be applied to ancestor-descendant relationships, or to infer the net selection implicated in the divergence of two extant species from a common ancestor8,‘6,‘7. Figure I shows three suggesting possible examples that: (f) Y has been subject to directional selection to increase; (2) Y has been subject to no net directional selection; (3) Y has been subject to directional selection to decrease.
Y
Case
O
2
Case 3
/
I
Ancestor X
Fig. 1. Selection on X results in a correlated response species can be of Y (line). Ancestral and descendant compared to determine the net force of selection acting directly on Y, given several assumptions (Box 2). The method can also be used to compare the minimum amount of direct selection implicated in the divergence of two extant species from a common ancesto&‘6,17. Three cases are illustrated, suggesting selection to increase Y (case I), no directional selection on Y (case 2) or selection to decrease Y (case 3).
308
Case I Y lies above the regression slope, suggesting that there has been direct selection to increase Y, and implying clear adaptive significance for Y in the descendant species. However, there are at least two ways by which Y may have evolved entirely by correlated response, even in this case. First, the genetic regression may have changed. While this is plausible, or even likely’8,‘9, no examples from comparative studies have been proposed in the context of correlated response, although Landes suggested that a reduced correlation genetic between brain and body size could have facilitated rapid independent evolution in some lineages. Second, another character correlated with Y may be subject to direct selection. This was suggested by Riska and Atchley’ as a means by which brain size could evolve continuously by correlated response to selection on body size, even though brain-body allometric relationships across orders are steeper than they are across within genera. The species essence of the idea is that selection to increase body size initially acts to change both cell size and cell number. AAer some response, additional direct selection opposes further increase in cell size, so that increases in body size are now largely to attributable increase in cell number. Body size variation via cell number may have a higher genetic correlation with brain size and hence produce a steeper correlated response than body size variation via cell size.
Case 2 Y lies on the regression slope, implying that it has been subject to no net directional selection, as would be the case if it were entirely neutral. However, this result may also occur if selection on X produces an optimal shift in Y. In this case, Y is subject to stabilizing selection in both ancestral and descendant species, and the two optima for Y lie on the genetic regression of Y on X (Fig. 2). One example comes from the brain:body studies. Lande8 demonstrated that within-genera across-species allometric relationships between brain and body could have arisen entirely by directional selection on body size. The result follows because different species lie on the genetic regression of brain on body, based on quantitative genetic studies in mice. Since any directional selection on brain size should cause a displacement of mean brain size from this regression slope, no directional selection on brain size is implicated. An alternative interpretation is that brain size has been subject to selection to both increase and decrease during the course of evolutionary divergence and that these amounts cancelled exactly. This hypothesis is difficult to assess using comparative methods. Brain size is not a neutral character, and mean brain size is likely to be close to that predicted on the basis of adaptive considerations’O. Presumably brain size is held at this position by stabilizing selection (Fig. 2). Evolution entirely by correlated response, which refers to forces of directional selection during an evolutionary transition, does not directly address the question of what maintains the character at its currently observed value (see below). It may seem remarkable that changes in one character should sometimes lead to optimal changes in another as a correlated response, and the extent to which this is really the case requires much more empirical study. It has been suggested that genetic correlations might themselves evolve in populations for adaptive allometric reasonsLo,2’. If this is correct,
TREE vol. 7, no. 9, September
the correlated response duce an approximately change, at least during stages of evolution.
1992
may prooptimal the early
Case 3 Y lies below the regression slope, implying that it has been wbject to directional selection to decrease, even if it has in fact increased during the course of evolution. As in the cases above, I his interpretation assumes that !.he genetic regression remains unI:hanged, and that no other charac*:ers are subject to direct selection. 4n example comes from studies of Darwin’s finches. The medium ground finch, Geospiza fortis, and the cactus finch, C. scandens, have similar beak depths, but very different beak lengths. Depth and length are positively genetically correlated22, implying that there has been strong selection against a change in beak depth as beak length evolved during the course of divergence of these two species from their common ancestoP. The unchanging beak depth is of as much adaptive significance as the increase in beak length. Evolution of maladaptive characters by correlated response Whenever characters are subject to selection, many other characters should evolve by correlated response. This has been demonstrated in numerous artificial selection
experiments. Mice selected for increased body size have reduced activity patterns23, and mice selected for differing levels of fat content have different bone structures24. One famous experiment involved selection of silver foxes for tameness over 20 generations25. Foxes were rated on a scale of 1-4 depending on levels of aggression and fear, and animals that consistently displayed tame behavior were selected for breeding (in the first generations, even these animals bit the investigators). Initially 90% of the animals were classified as aggressive and/or fearful, but by the eighteenth generation all animals were actively seeking human contact. Correlated changes included uttering dog-like sounds, wagging tails, drooping ears, piebald patterns, females going into estrus twice a and elevated serotonin year, (5-HT) levels in the brain25. Many of these features have been interpreted as juvenile-like characteristics which have appeared as a side effect of changing hormone concentrations25~26. On the basis of this experiment and comparative studies, Coppinger and Feinstein” have recently suggested that the barking of dogs is not adaptive, and never was. There are three distinct ways by which characters that have evolved mainly by correlated response can continue to persist in populations.
The first is if the correlated character is at a new optimum and maintained there by stabilizing selection (Fig. 2). The second is if the character is neutral or of very little adaptive significance, such that selection modifying its expression is very weak. Examples may include barking dogs and many cases of traits expressed vestigially in one sex, such as the male nipple15.
Y
X Fig. 2. Even characters of great adaptive significance can evolve entirely by correlated response, and not be subject to any net directional selection. The genetic regression of Y on X is given by the solid line, and is the predicted trajectory for the evolution of Y (e.g. brain size) if the environment changed to favour a new mean value of X (e.g. body size). In this example Y is everywhere subject to strong stabilizing selection (as indicated by arrows which point in the direction of increased fitness for Y at given X values, and the dotted lines which represent hypothetical individual fitness contours). The example has been constructed such that the optimal value of Y increases with X, and lies on a ridge that coincides with the regression line. Any correlated response in Y will not die away, but will be permanently maintained by stabilizing selection.
309
TREE vol. 7, no. 9, September
The third way by which correlated responses can continue to persist is if each correlated trait is subject to genetic variation that is entirely pleiotropic. Then each trait may never evolve to its optimum, even if selection is strong. There are many cases of strikingly maladaptive traits persisting as a result of correlated response, most strikingly from the literature on life-history trade-offs27’28. One example is senescence, which may have no adaptive value itself. A popular is that it persists hypothesis because genetic variation causing senescence has pleiotropic effects, increasing fecundity at young ages2”,“. It has been recently emphasized that even low genetic correlations among pairs of traits may be sufficient for whole suites of traits to be permanently held far from their optimal values2’,‘“. Each trait shares some genetic variation with one or more of the other traits, and no single trait is governed by variation unique to it. Empirically this finding creates the problem that measurements between a few of the traits may reveal low genetic correlations, suggesting that each trait can be separately optimized, although a consideration of the whole organism would show all traits to be highly constrained27,2”. Correlated responses and behavior correlated response Recently, has been used to explain the presence of several behavioral traits: kin recognition (correlated with recognition sysspecies tems)” ‘I; multiple mating by females (correlated with multiple mating by males)“; and helping at the nest by individuals who not parents (correlated are with parental provisioning)‘2,32. Because the inferred targets of direct selection seem to be of such obvious adaptive significance, and correlations likely, the absence of kin recognition, female multiple mating, or helping may be at least as interesting as its presence. Distinguishing correlated response from direct selection is likely to be particularly important in behavioral studies. Because behavioral traits are than more readily observed 310
morphological or physiological traits, behaviors with potentially weak effects on fitness are more commonly investigated. Such behaviors may either take a very long time to disappear from a population, or may be permanently maintained as a result of pleiotropy. What strategies can be used to determine whether traits are present primarily because they are correlated with other traits? One needs to identify those correlated traits that are the potentially important direct targets of selection. This can be difficult; in some cases, such traits may actually be absent from the contemporary population. For example, there is strong selection to eject a brood parasite’s eggs from a bird’s own nest”. As a correlated response birds may reject their own and this behavior has eggs”,‘“, been shown to persist in contemporary populations even after the brood parasite has become extincP5. If traits that are potentially important in producing correlated changes can be identified, we suggest that correlated response is set up as the null hypothesis. Ways in which the behavior has been subsequently modified, if at all, can then be considered using standard approaches such as cost-benefit analysis2j. It is worth re-emphasizing two points. First, in some instances, traits common to many species but not present in the behavioral repertoire of a particular species may be of more significance, and more worthy of investigation, than those behaviors, however bizarre, that are held in common across all species in a group. The absence of a behavior from one particular species may imply there has been selection for its loss, whereas the presence of similar behaviors (e.g. helping at the nest) across many species may reflect correlated responses to a genselection pressure (e.g. eral parental feeding). Second, selection on many correlated traits will generally shape the form of any particular trait. Many behaviors will only make sense when considered in the context of the whole phenotype.
1992
Acknowledgements We thank I. Billick, T. Case, M. Hack. K. Hanley, L. Liou, K Marchetti, L. Rowe, T. Wright and the reviewers for advice.
References
I Wright, S. ( 1980) Evolution 34, 825-843 2 Gould, S.J. I 1983) Evolution 37, 856-858 3 Darwin, C. f 1889) The Origin of Species by Means of Natural Selection, Appleton 4 Reeve, E.C.R. (1960) Cenet. Res I, 151-172 5 Lewontin, R.C (1972) Nature 236, 181-182 6 Could, S.J. and Lewontin, R.C. (1979) Proc. R. Sot. London Ser. B 205. 581-598 7 Sober, E. ( 1984) The Nature of Selection, MIT Press 8 Lande, R. (1979) Evolution 33, 402-416 9 Riska, B and Atchley, W.R. I19851 Science 229, 668-671 10 Pagel, M.D. and Harvey, P.H. (19891 Science 244, l58?-I 593 I I Halliday. T. and Arnold, S.J. (19871 Anim. Behav. 35,939-94 I I2 lamieson, I G. (19891 Am Nat. 133. 394-406 13 Crafen, A 119901 Anim. Behav iY, 42-54 14 Kirkpatrick, M. and Ryan, M.1 (1991) Nature 350, 33-38 I5 Lande, R. (19801 Evo/ufion 34, 292-305 16 Price, T.D Grant, P.R. and Boag, P.T. ( 1984) in Population Biology and Evolution (Wahrmann, K and Loeschke, VI edsl. pp. 49-66, Springer-Verlag 38, 17 Schluter, D ( I9841 Evolution 921-930 I8 Turelli, M. (19881 Evolution 42, 1442-1347 I9 Wilkinson, G S., Fowler, K and Partridge, L. (19901 Evolution 44, 1990-2003 20 Cheverud, I. ( I9841 / rheor. Biol. I IO, 155-171 21 Schluter, D. and Smith, 1N.M. (1986) Biol I. Linn. Sot. 29, 23-36 22 Boag, P.T. ( I9831 Evolution 37, 877-894 23 Falconer. D.S. II951 I /. Genet. 51, 470-50 I 24 Atchley, W.R. et al (IY901 Evolution 44, 669-688 25 Belyaev, D.K. I IQ791 / Hered. 70, 30 I-308 26 Coppinger, R. and Feinstein, M. (I991 J Smithson. Annu. 2 I, I 19-l 29 27 Pease, C.M and Bull, 1.1. 11988) /. Evol. Biol. I, 293-303 28 Charlesworth, 520-538
B.
I 1990)
Evolution
44,
29 Williams, C.C. (1957) t‘volution I I, 398-4 I I 30 Rose, M.R. (lY91 I The Evolutionary Biology ofAging, Oxford University Press 31 Barnard, C. (I991 I Trends Ecol Evol h. 310-312 32 Mumme. R.L. and Koenig, W.D. (lY91 I Trends Ecol. Evol 6, 343-344 33 Davies. N.B. and Brooke, M. de L ( I9881 Anim. Behav 36, 262-284 34 Marchetti, K.E 119921 Proc. R Sot London Ser. B 248, 4 I-45 35 Emlen, S.T. et a/. ( 199 I ) Am. Nat. I 38, 259-270 36 Bulmer, M.C. ( 1972) Cenet. Res 19, 17-25 37 Shaw R.G (1991) Evolution45, 141-151
7, no. 9, September
1992
( I’-19 I) Evol. Trends Plants 5, 109-I 23 28 Rothera, S.L. and Davy, A.I. (I 986) New Phytol. 102, 449-467 29 Brammal, R.A. and Semple, I.C. ( 19901 Can. I. BoT. 68, 2065-2069 30 Van Dijk, P., Hartog, M. and Van Delden, W. Biol /. Linn. Sot. (in press) 31 Stebbins, G.L. (19851 Ann. MO. Bat. Card. 72,824-832 32 Roose, M.L. and Cottlieb, L.D. (1976) E\,o/otion 30, 8 18-830 33 Shore, I.S. (1991) Heredity66, 305-321 34 Krebs, S.L. and Hancock, J.F. (1989) Heredity63, I I-18 35 Soltis, D.E. and Rieseberg, L.H. (19861 Am. /. Bat. 73, 3 I O-3 I8 36 Novak, S.I., Soltis, D.E. and Soltis, P.S. ( I 39 I ) Am. /. Bot. 78, 1586-l 600 37 Samuel, R., Pinsker, W. and Ehrendorfer,
F. ( I9901 Heredity 65, 369-378 38 Tomekpe, K. and Lumaret, R. (1991) Evolution 45,359-370 39 Thompson, I.D.. McNeilly, T. and Gray, 117, 141-152 A.j. (1991) NewPhytol. 40 Thompson, I.D. ( I99 I) Bioscience
4 I,
393-40 I 41 Macdonald,
S.E., Chinnappa, C.C. and Reid, D.M. (1988) Evolution 42, 1036-1046 42 Garbutt, K. and Bazzaz. F.A. (1983) New Phytol. 93, 129-l 41 43 Bever, I.D. and Felber, F. Oxf Sorv Evol. Biol. (in press) 44 McElroy, A.R. (1991) Euphytica 55, 117-123 45 Quarin, C.L. and Hanna, W.W ( 1980) Crop Sci. 20, 69-75 46 Marks, G.E (1966) Evolution 20, 552-557 47 Barrett, S.C.H. (19891 in Speciation and
Evolution
its Consequences (Otte, D. and Endler, J.A., eds), pp. 257-283, Sinauer 48 Ganders, F.R. (1989) in Genetics, Speciation and the Founder Principle (Giddings, L.V., Kaneshiro, K.Y. and Anderson, W.W., eds), pp. 99-l 12, Oxford University Press 49 Marshall, D.R. and Brown, A.H.D. (1981) Heredity32. 321-323 50 Normann, G.A. and Quarin, C.L. (1987) Cenome 29,340-344 M.D. (1991) 51 Wetth, C.R. and Windham. Am. Nat. I37,5 15-526 52 Pernes, 1. ( 1984) Gestion des Ressources CCnPtiques des Plantes, Tome 2: Manuel, Lavoisier 53 Endler, 1.A. (1989) in Speciation and its Consequences (Otte, D. and Endler, ].A., eds), pp. 625-648, Sinauer
of Correlated
Characters
Trevor Price and Tom Langen Muny traits are genetically correlated with each other. fius, selection that changes the mean value of one trait causes other traits to change as well. Recent comparative studies have emphasized the pxsible importance of such correlated rc!sponses in affecting the evolution of traits, including some Gehviors, which are of little adaptive significance, or even maladaptive. However, it is also possible for traits with major effects on fitness, srrch as brain size, to evolve entirely 6y r,?rrelated response. Other traits that do riot appear to have evolved at all may IIave been subject to much directional selection, simply to prevent their evolil tion by correlated response. The new i qterest in correlated responses reflects rqore rigorous attempts to consider the crganism as a whole, rather than dissectieg it into a num6er of questionably sepI:lrable traits. There are two main ways by which characters of no adaptive Ggnificance can evolve: genetic drift, and the correlated response IO selection on other characters. Correlated responses arise through pleiotropy (the multiple effects of individual genes) and linkage disequilibrium (nonrandom associ&ion between alleles at different :oci). Pleiotropy, in particular, is ‘Nidespread’, so correlated re~;ponses should be common. rrevor Price and Tom Langen are at the Dept of 3iology, 01 16, University of California at San Diego, _a lolla, CA 92093, USA. B 1992, Elsev~er Science Publishers
Ltd (UK)
Indeed, Sewall Wright’, who is perhaps better known for his theories involving genetic drift, thought that nonadaptive character differences among species (if they occur at all) are mostly attributable to pleiotropy and correlated response. The idea of correlated response is not new, being found in the earliest known coherent formulation of natural selection (see Ref. 2). It was discussed extensively by Darwir?, and is still regularly considered in discussions of neutral evolution, and in criticisms of pan-selectionism4-7. Correlated response has recently been discussed in two main contexts: the evolution of brainbody allometric patternPa, and the evolution of several different kinds of behaviors”-‘4. Each has engendered much controversy. Here, we review correlated response and discuss the way in which it relates to common ideas of adaptive evolution. We make three points. All have been made before, but each has also been overlooked in some recent discussions. First, a character whose interspecific variation is thought to be of major adaptive significance based on comparative or functional studies (e.g. relative brain size) may have evolved from some ancestral state entirely by
correlated response - evolution by correlated response does not necessarily imply neutrality. Secondly, characters that show no variation among species may nonetheless have been subject to much directional selection, otherwise they would have evolved as a consequence of genetic correlations with other characters that do differ among the species. In such cases, special reasons are needed to explain why these traits have not evolved. Thirdly, genetic correlations can greatly slow the evolution of weakly selected characters toward their optima15, and traits that are of little adaptive significance, or even strongly maladaptive, can persist indefinitely as a result of selection on other correlated traits. Identifying correlated responses The basic concept of correlated response can be illustrated with a simple genetic model (Box I ). When selection is applied to a single character, X, in some ancestral population, a second character, Y, evolves along a slope given by the additive genetic regression of Y on X (Fig. I). When selection is applied to Y but not X the population evolves along a slope given by the additive regression of X on Y. Any deviation from these 307
TREE vol. 7, no. 9, September
1992
Box 1. Correlate The
essenti
response can I plified modal 0J ation, adapted 1
below illustrate9/ characters, X d character is ei by many gen&a Assume that th genes: ‘A’ gene&:. pleiotropic) whc affect either X &%F.J there are equal class and all a same. Selection X by 1 unit leadi
due to A genes genes by 0.5 uni B genes onfy A?
slopes implies that both characters have been subject to some directional selection, given several assumptions (see below). The minimum amount of selection on each character can be determined using the method of LandeB I6 (Box 2). The method can compare be applied to ancestor-descendant relationships, or to infer the net selection implicated in the divergence of two extant species from a common ancestor8,‘6,‘7. Figure I shows three suggesting possible examples that: (f) Y has been subject to directional selection to increase; (2) Y has been subject to no net directional selection; (3) Y has been subject to directional selection to decrease.
Y
Case
O
2
Case 3
/
I
Ancestor X
Fig. 1. Selection on X results in a correlated response species can be of Y (line). Ancestral and descendant compared to determine the net force of selection acting directly on Y, given several assumptions (Box 2). The method can also be used to compare the minimum amount of direct selection implicated in the divergence of two extant species from a common ancesto&‘6,17. Three cases are illustrated, suggesting selection to increase Y (case I), no directional selection on Y (case 2) or selection to decrease Y (case 3).
308
Case I Y lies above the regression slope, suggesting that there has been direct selection to increase Y, and implying clear adaptive significance for Y in the descendant species. However, there are at least two ways by which Y may have evolved entirely by correlated response, even in this case. First, the genetic regression may have changed. While this is plausible, or even likely’8,‘9, no examples from comparative studies have been proposed in the context of correlated response, although Landes suggested that a reduced correlation genetic between brain and body size could have facilitated rapid independent evolution in some lineages. Second, another character correlated with Y may be subject to direct selection. This was suggested by Riska and Atchley’ as a means by which brain size could evolve continuously by correlated response to selection on body size, even though brain-body allometric relationships across orders are steeper than they are across within genera. The species essence of the idea is that selection to increase body size initially acts to change both cell size and cell number. AAer some response, additional direct selection opposes further increase in cell size, so that increases in body size are now largely to attributable increase in cell number. Body size variation via cell number may have a higher genetic correlation with brain size and hence produce a steeper correlated response than body size variation via cell size.
Case 2 Y lies on the regression slope, implying that it has been subject to no net directional selection, as would be the case if it were entirely neutral. However, this result may also occur if selection on X produces an optimal shift in Y. In this case, Y is subject to stabilizing selection in both ancestral and descendant species, and the two optima for Y lie on the genetic regression of Y on X (Fig. 2). One example comes from the brain:body studies. Lande8 demonstrated that within-genera across-species allometric relationships between brain and body could have arisen entirely by directional selection on body size. The result follows because different species lie on the genetic regression of brain on body, based on quantitative genetic studies in mice. Since any directional selection on brain size should cause a displacement of mean brain size from this regression slope, no directional selection on brain size is implicated. An alternative interpretation is that brain size has been subject to selection to both increase and decrease during the course of evolutionary divergence and that these amounts cancelled exactly. This hypothesis is difficult to assess using comparative methods. Brain size is not a neutral character, and mean brain size is likely to be close to that predicted on the basis of adaptive considerations’O. Presumably brain size is held at this position by stabilizing selection (Fig. 2). Evolution entirely by correlated response, which refers to forces of directional selection during an evolutionary transition, does not directly address the question of what maintains the character at its currently observed value (see below). It may seem remarkable that changes in one character should sometimes lead to optimal changes in another as a correlated response, and the extent to which this is really the case requires much more empirical study. It has been suggested that genetic correlations might themselves evolve in populations for adaptive allometric reasonsLo,2’. If this is correct,
TREE vol. 7, no. 9, September
the correlated response duce an approximately change, at least during stages of evolution.
1992
may prooptimal the early
Case 3 Y lies below the regression slope, implying that it has been wbject to directional selection to decrease, even if it has in fact increased during the course of evolution. As in the cases above, I his interpretation assumes that !.he genetic regression remains unI:hanged, and that no other charac*:ers are subject to direct selection. 4n example comes from studies of Darwin’s finches. The medium ground finch, Geospiza fortis, and the cactus finch, C. scandens, have similar beak depths, but very different beak lengths. Depth and length are positively genetically correlated22, implying that there has been strong selection against a change in beak depth as beak length evolved during the course of divergence of these two species from their common ancestoP. The unchanging beak depth is of as much adaptive significance as the increase in beak length. Evolution of maladaptive characters by correlated response Whenever characters are subject to selection, many other characters should evolve by correlated response. This has been demonstrated in numerous artificial selection
experiments. Mice selected for increased body size have reduced activity patterns23, and mice selected for differing levels of fat content have different bone structures24. One famous experiment involved selection of silver foxes for tameness over 20 generations25. Foxes were rated on a scale of 1-4 depending on levels of aggression and fear, and animals that consistently displayed tame behavior were selected for breeding (in the first generations, even these animals bit the investigators). Initially 90% of the animals were classified as aggressive and/or fearful, but by the eighteenth generation all animals were actively seeking human contact. Correlated changes included uttering dog-like sounds, wagging tails, drooping ears, piebald patterns, females going into estrus twice a and elevated serotonin year, (5-HT) levels in the brain25. Many of these features have been interpreted as juvenile-like characteristics which have appeared as a side effect of changing hormone concentrations25~26. On the basis of this experiment and comparative studies, Coppinger and Feinstein” have recently suggested that the barking of dogs is not adaptive, and never was. There are three distinct ways by which characters that have evolved mainly by correlated response can continue to persist in populations.
The first is if the correlated character is at a new optimum and maintained there by stabilizing selection (Fig. 2). The second is if the character is neutral or of very little adaptive significance, such that selection modifying its expression is very weak. Examples may include barking dogs and many cases of traits expressed vestigially in one sex, such as the male nipple15.
Y
X Fig. 2. Even characters of great adaptive significance can evolve entirely by correlated response, and not be subject to any net directional selection. The genetic regression of Y on X is given by the solid line, and is the predicted trajectory for the evolution of Y (e.g. brain size) if the environment changed to favour a new mean value of X (e.g. body size). In this example Y is everywhere subject to strong stabilizing selection (as indicated by arrows which point in the direction of increased fitness for Y at given X values, and the dotted lines which represent hypothetical individual fitness contours). The example has been constructed such that the optimal value of Y increases with X, and lies on a ridge that coincides with the regression line. Any correlated response in Y will not die away, but will be permanently maintained by stabilizing selection.
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The third way by which correlated responses can continue to persist is if each correlated trait is subject to genetic variation that is entirely pleiotropic. Then each trait may never evolve to its optimum, even if selection is strong. There are many cases of strikingly maladaptive traits persisting as a result of correlated response, most strikingly from the literature on life-history trade-offs27’28. One example is senescence, which may have no adaptive value itself. A popular is that it persists hypothesis because genetic variation causing senescence has pleiotropic effects, increasing fecundity at young ages2”,“. It has been recently emphasized that even low genetic correlations among pairs of traits may be sufficient for whole suites of traits to be permanently held far from their optimal values2’,‘“. Each trait shares some genetic variation with one or more of the other traits, and no single trait is governed by variation unique to it. Empirically this finding creates the problem that measurements between a few of the traits may reveal low genetic correlations, suggesting that each trait can be separately optimized, although a consideration of the whole organism would show all traits to be highly constrained27,2”. Correlated responses and behavior correlated response Recently, has been used to explain the presence of several behavioral traits: kin recognition (correlated with recognition sysspecies tems)” ‘I; multiple mating by females (correlated with multiple mating by males)“; and helping at the nest by individuals who not parents (correlated are with parental provisioning)‘2,32. Because the inferred targets of direct selection seem to be of such obvious adaptive significance, and correlations likely, the absence of kin recognition, female multiple mating, or helping may be at least as interesting as its presence. Distinguishing correlated response from direct selection is likely to be particularly important in behavioral studies. Because behavioral traits are than more readily observed 310
morphological or physiological traits, behaviors with potentially weak effects on fitness are more commonly investigated. Such behaviors may either take a very long time to disappear from a population, or may be permanently maintained as a result of pleiotropy. What strategies can be used to determine whether traits are present primarily because they are correlated with other traits? One needs to identify those correlated traits that are the potentially important direct targets of selection. This can be difficult; in some cases, such traits may actually be absent from the contemporary population. For example, there is strong selection to eject a brood parasite’s eggs from a bird’s own nest”. As a correlated response birds may reject their own and this behavior has eggs”,‘“, been shown to persist in contemporary populations even after the brood parasite has become extincP5. If traits that are potentially important in producing correlated changes can be identified, we suggest that correlated response is set up as the null hypothesis. Ways in which the behavior has been subsequently modified, if at all, can then be considered using standard approaches such as cost-benefit analysis2j. It is worth re-emphasizing two points. First, in some instances, traits common to many species but not present in the behavioral repertoire of a particular species may be of more significance, and more worthy of investigation, than those behaviors, however bizarre, that are held in common across all species in a group. The absence of a behavior from one particular species may imply there has been selection for its loss, whereas the presence of similar behaviors (e.g. helping at the nest) across many species may reflect correlated responses to a genselection pressure (e.g. eral parental feeding). Second, selection on many correlated traits will generally shape the form of any particular trait. Many behaviors will only make sense when considered in the context of the whole phenotype.
1992
Acknowledgements We thank I. Billick, T. Case, M. Hack. K. Hanley, L. Liou, K Marchetti, L. Rowe, T. Wright and the reviewers for advice.
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