TREE vol. 3,
effects for fertility differentials may be an enormous and nearimpossible task29,31. Prospects From theoretical investigations it appears that certain types of fertility selection can give rise to different genetic dynamics than viability selection. Obviously not all fertility selection will be of these types, and not all fertility selection will be strong enough to make a difference. However, there are enough data available to suggest that fertility selection is often not negligible, and may often take on the complex forms that can produce novel genetic dynamics. The salient variables that determine the role of fertility selection are well defined by theory. There are real difficulties in estimating the strength of fertility selection, and we may never be able to understand the detailed genetics of fertility effects. Nevertheless, the potential importance of such effects seems compelling enough to suggest that the field devote the same intensity of effort to the study of fertility selection
that has been devoted to viability and sexual selection.
Acknowledgements I thank Dr M.W. correcting my errors offering suggestions particular emphasis. are my own, and the is mine. My research al Science Foundation
Feldman for patiently in a previous draft and for topics deserving Any remaining errors final choice of emphasis is supported by Nationgrant BSR 84- 15529.
References
I Sober, E. ( 1984) The Nature of Selection. MIT Press 2 Manly, B.F.I. ( 1985) The Statistics of Natural Selection. Chapman and Hall 3 Endler, 1.A. 11986) ~VaCura/Se/ecCion in the Wild, Princeton University Press 4 Hedrick, P.H. 119831 Genetics of Populations, Science Books International 5 Feldman, M.W., Christiansen, F.B. and Liberman.U.119831 Genetics 105, 1003-1010 6 Hadeler, K.P. and Liberman, U. ( 19751 I. Math. Biol. 2. 19-32 7 Prout, T. I I965 1Evolution I9,546-55 I 8 Clark, A.G.and Feldman, M.W. t 1981 I Heredity 46, 347-377 9 Simmons, M.I. and Crow, J.F II9771 Annu. Rev. Genet. I I, 49-78 IO Prout, T. (I971 1 GeneCics68, 127-149 I I Clark, A.C. and Doane, W.W. f I9841 Evolution 38,957-982 I2 Beckenbach, A. 119831 Am. Nat. I2 I, 630-648
InbreedingAvoidanceBehaviors Sharon Forster Blouin and Michael Blouin Inbreeding is defined as mating between individuals related by common ancestry. Thus, the degree to which a particular mating is in6red depends on how far back in a pedigree one 6egins counting common ancestors. In general practice, the term inbreeding is used to describe mating between close relatives (first cousins or closer). Animal breeders have hnown for centuries that in6reeding causes a loss of constitutional vigor and fertility in domestic livestock. A growing literature now demonstrates that the offspring of matings between close relatives in species of undomesticated birds and mammals are less fit than out6red offspring’. The deleterious consequences of in6reeding suggest the possibility that many species have evolved behaviors that lower the frequency of inbreeding.
Sharon Forster Blouin and Michael Blouin are at the Department
sity, Tallahassee,
230
of Biology, Florida State UniverFL. 32306-2043, USA.
The existence of inbreeding avoidance behaviors is inferred from the ill effects of inbreeding, from the paucity of examples of close inbreeding in nature’, and from electrophoretic surveys that fail to find excess homozygosity in species having prolonged contact between close relatives34. The reader is encouraged to consult Moore and Ali’, Greenwooda, Dobson and Jonesg, Puseylo, and especially Rails et a/.2 for further review of purported avoidance behaviors and their evolution. Behaviors reported to function as inbreeding avoidance mechanisms fall into two classes: those in which dispersal reduces contact between relatives; and those in which animals with access to close kin avoid mating with them. Dispersal as an inbreeding avoidance mechanism has been reviewed recently in TREElO. Examples of the second
no.
9,
September
1988
I3 O’Donald, P. and Davis. I.W.F. II9761 Heredity 36,343-350 I4 Berven. K.A. 11982) Evolution 36,962-98’s I5 Kalisz, S. 119861 Evolution 40,479-491 I6 Schmidt, K.P. and Levin, D.A. f 19851 Evolution 39,396-404 I7 Cothran, E.G., Chesser, R.K.. Smith. M.H. and fohns. P.E. ( 1983 I Evolution 37, 282-29 I I8 Shrode, J.B. and Gerking. SD. I 1977) Physiol. Zoo/. 50, l-l 0 I9 Robbins, L. and Travis, I I 19861 Am. Nat 128.409-415 20 Kynard, B.E. ( 19781 Behaviour67. 178-207 21 Downhower. I.F. and Brown, L. (1980) Anim. Behav. 28,728-734 22 Feldman, M.W and Liberman, U. II9851 Genetics, 109,229-253 23 Holsinger, K.E.. Feldman, M.W. and Altenberg, L. II9861 Genetics I I2,909-922 24 Pollak, E. 11978) Cenetics90,383-389 25 Nagylaki, T. f 19791 Ann. Hum Genet. 41. 143-150 26 Abugov, R. I I9851 I Theor. Biol I 11. 109-125 27 Abugov, R II9861 I Theor Rio/ i 71, 31 i-323 28 Travis, I. and Henrich. S 119861 Evolution 40.786-790 29 Sved. I.A. and Ayala, i- 1 I 19701 Genetics 66,97-l I3 30 Siegismund, H.R and Christiansen. F.K I I985 I Theor. Popul. Biol. 27,268-297 31 Lewontin. R.C. t 19741 The Genetic Basis of Evolutionary Change, Columbia University Press 32 Penrose, L.R. I 19491 Ann Eugen 11, 30 l-304 33 Bodmer, W.F II9651 Genetics 5 I, 11l-424
class of avoidance behaviors fall into three partially overlapping categories: first, where parents suppress offspring sexuality; second, where siblings make qoor partners; and third, where mate choice actively favors non-kin. Parents suppress offspring sexuality Individuals may delay sexual maturity or lack sexual motivation as long as they remain with their parents. Loss of reproductive activity in subordinate members of mammalian social groups is a common phenomenon that is manifest in a variety of ways such as reduction of testis size in males and resorption or abortion of embryos, and failure to cycle regularly in femalesi’,12. For example, in several species of callitrichid monkeys (marmosets and tamarins) only the dominant female in a social group reproduces’ 1,i2. Epple and Katz” showed that estrogen excretion and ovarian cycling is repressed in young female saddle back tamarins (Saguinus fuscicollisl as long as they remain with their natal family
‘REE vol. 3, no. 9, September
1988
Table1.Examples ofconditional breeding Female bred first year
Prairie dogs5 i;roup or are exposed to the group’s odor. Such inhibitions obviously reduce inbreeding when groups contain related individuals. An ;Ilternative explanation for reduced !;exual activity is to avoid aggres4on from older, sexual competitors ._ particularly among males when lemales are a limited resource las in most mammals)L3. Similar repression might occur among females of species with substantial paternal care or when a sub;)rdinate female’s offspring would resources with :,ompete for ,:)ffspring of the dominant female. A particularly convincing argument for inbreeding avoidance as ?he ultimate cause of sexual repres:.ion is provided by three examples of loss of inhibition only when the I.)pposite sex parent is absent or replaced (Table I). Although most remale prairie dogs (Cyonomys iodovicianus) breed in their second h’ear, after the father has left the family group, a few will reach maturIty in their first year5. Hoogland5 tgund that a lower percentage of b’earling females reached sexual maturity in the presence of their tather than when the father was ;: bsent. ArmitageLJ reports similar results from female yellow-bellied marmots (Marmota f7aviventrisl. F‘inally, although mature offspring (If the communally-nesting acorn formiciwoodpecker (Melanerpes \,orus) usually fail to breed in a nest containing both parents, they will I-breed if the opposite sex parent is replaced 15. Siblings make poor partners The second type of evidence for kin avoidance is the low reproductive rate of paired siblings. Zookeepers and others interested i I breeding birds and mammals know that allowing juveniles of some species to associate freely can interfere with breeding behavior at maturity. At least seven studies of four rodent species suggest that when sibling littermates are paired they initiate reproduct on later and/or have a lower rate cf offspring production than do Faired unfamiliar animals’“20. E:ven the smell of male voles LMicrotus ochrogasterl can inhibit sexual behavior in their female siblings19. Delayed and infrequent offspring F:lroduction can be explained as in-
Yellow-bellied marmotsI
Female bred first year
Female year
Acorn woodpeckers15
Offspring stayed and bred
parent still in
in natal nest la
parent absent
8
not
breed
first
did
not
breed
first
9 28
1 19
Father present Father absent
did
26 3;’
2 13
Father present Father absent
Opposite-sex nest Opposite-sex
Female year
Offspring breed
st,ayed but did not 39” 2
alnferred from the number of eggs laid in a nest (see Fig. 2 in Ref. 15). bFour cases direct observation; 35 cases inferred from number of eggs laid in nest (see Fig. 2 in Ref. 15).
breeding depression in studies that simply compare the performance of paired relatives to that of paired non-relatives. However, Hill’sI crossfostering experiments maniculawith mice (feromyscus tusl showed that paired littermates reproduce later than paired strangers, regardless of relatedness (i.e. sibs behaved like strangers when reared apart and unrelateds behaved like sibs when reared together). Agren’ 7 reports similar results using Mongolian gerbils (Meriones unguiculatus). HillI suggests that delayed reproduction is an inbreeding avoidance mechanism because it extends the period during which unfamiliar mates can be obtained. Matechoice The third category is active mate choice favoring non-kin. Females of normally monogamous Mongolian gerbil pairs visit neighboring males to copulate though they return to their mates (often siblings) to bear and raise their litters. Furthermore, pairs formed from unfamiliar indipairs viduals persist whereas composed of individuals raised together are unstablet7. Packer21 observed that female olive baboons (Papio anubis) mate with immigrants to their natal troop significantly more often than with resident males who may be relatives. Young adult male and female lions also appear less willing to mate with members of their natal pride than with strangers22. Similarly, immature female chimpanzees (Pan troglodytes) have a preferred male (usually a sibling) with whom they spend most of their time23. At
maturity the female abandons the company of the male and these previously preferred males rank significantly lower than the median male in the number of times each copulates with the female23. Finally, unrelated humans raised to adulthood in communal nurseries are disinclined to form adult sexual relationships24, and the obsolete Taiwanese practice of raising bride and groom together resulted in reluctance to marry and in more sexual and marital dissatisfaction than do other forms of arranged marriage25. How does juvenile association interfere with reproduction later on? It has been suggested that if individuals of social species form one type of bond or establish a set of behaviors towards each other, it is then difficult for them to establish new bonds or to engage in new behaviors towards each other26. For example, familiar voles do not perform the naso-genital grooming behavior that is necessary to transfer pheromone physically and induce female reproductive activityIn. Two additional behaviors could conceivably function as inbreeding avoidance by mate choice. The first is ‘rare male advantage”’ in which females actively choose males bearing the most uncommon phenotype. Female guppies (Poecilia reticulata) preferentially mate with males bearing whichever of several Y-linked color variants happens to be rare in the population28. Farr28 hypothesized that this preference serves to maximize outcrossing in a species that frequently colonizes ephemeral habitats and may be subject to population bottlenecks 231
TREE vol. 3, no. 9, September
and frequent bouts of inbreeding. Indeed, lacy*9 showed mathematically that choice of rare males maximizes the fitness of a female’s offspring in a heterotic system. A second, more bizarre form of mate choice may occur when female rodents terminate their own reproductive effort and become receptive again after exposure to a novel male (the Bruce effect). For example, the smell or presence of a strange male blocks implantation in female mice (MIS muscu/us)~O and the presence of an unfamiliar male can terminate pregnancy in female prairie voles (Microtus ochrogaster) up to the 15th day of gestation (well after implantation 13’. Reproductive termination might be simply an unavoidable side effect of the noncyclic, male-induced estrous in Microtus3’ but this is an unsatisfactory explanation for the response in mice. One explanation is that pregnancy block is a pheromonally mediated30 male strategy for mate acquisition to which females have not yet evolved a defense. Alternatively, it might be an outcrossing device. If the group structure of territorial rodent species limits a female’s choice of mates mainly to relativesIb, then automatically trading ‘one in the hand’ for the opportunity to outcross may be a selected strategy.
Discussion In some
verbal models it has been proposed that a moderate level of inbreeding is advantageous because it maintains favorable complexes of interacting alleles that would be disrupted by mating with a genetically very different mate3*. This disruption or ‘outbreeding depression’ has been documented in crosses between genetically divergent populations, but there is little evidence that it occurs in crosses between animals from the same population33. In addition, the models predict a preference among animals to mate with relatives but purported examples of such preference are quite controversial*. Though it is conceivable that inbreeding may be selectively advantageous in some situations, empirical evidence for this is scarce. In contrast, inbreeding depression is an indisputable phenomenon and one expects
selection to favor behaviors that reduce its frequency. Which are the most important avoidance behaviors? The examples of kin avoidance discussed above are less controversial than dispersal as an inbreeding avoidance mechanism2,7-9. This is not surprising when one weighs the costs of each class of mechanism. The rigors of dispersal may make kin recognition the cheapest solution to the inbreeding diIemma7J4. Species may, of course, employ several mechanisms to avoid inbreeding5. For example, differential dispersal by sex may separate siblings’0 while a kin recognition and avoidance system prevents parent-offspring mating. When should one see avoidance mechanisms? Because inbreeding is most deleterious between close relatives the degree of avoidance should be inversely proportional to relatedness. Indeed, reviewed examples focus on sibling and parent-offspring matings. Recent optimization models have examined the conditions under which inbreeding should be tolerated (reviewed by Waser et a1.34). Variables usually considered are the costs of the avoidance behavior to males and females, the loss of fitness owing to inbreeding depression (including the loss of inclusive fitness through a relatives’ reproductive failure) and the breeding system. The models conclude that, in general, inbreeding should be tolerated when the costs of avoidance are high and when an individual forfeits few outbred matings by choosing to inbreed. This second condition results in the prediction that male mammals should tolerate more inbreeding than females because the number of offspring a male sires is usually limited by the number of mates he can attract, while a female’s reproductive output is more limited by energetic or environmental constraints34. Empirically, there does not appear to be a bias towards either sex in the behaviors reviewed above. Do taxon-specific patterns of avoidance behaviors exist? Social birds, primates and rodents provide most examples. One might expect inbreeding avoidance to evolve under conditions of sociality
7988
where kin are apt to be in continued close contact. However, quantifying inbreeding or its avoidance requires multi-generation observations of numerous marked individuals. For practical reasons these data usually result from research on social species, which may explain the bias. Further studies are required to reveal whether inbreeding avoidance mechanisms are an integral part of most species’ behavioral repertoires.
References I Rails, K.and
Ballou, j 11983) in Genetics and Conservation ISchonewald-Cox, C.M., Chambers, S., MacBryde. B. and Thomas, L., edsf. pp. 164-184, Benjamin/Cummings Publishing Co., Inc. 2 Rails, K., Harvey, P.H.and Lyles, A.M. ( 19861 in Conservation Biology: The Science ofscarcityand Diversity ISoule,M., ed.), pp. 35-36. Sinauer Associates, Inc. 3 lohnson, M.S. and Brown, f.L (19801 Behav &co/. Sociobiol. 7, 93-98 4 Schwartz, O.A. and Armitage. K.B. II9801 Science 207,665-667 5 Hoogiand, I.L. ( 19821 Science 215. 1639-1641 6 Duncan, P., Feh. C, Cieize. f.C., Malkas, P and Scott, A.M. f 19841 Anim. Behav. 32. 520-527 7 Moore, I and Ali, R. ( I9841 Anim. Behav. 32. 94-l 12 8 Greenwood, P.]. II9831 in 7’he Ecologyof AnimalMovementfSwingiand. I. and Greenwood, P., edst, pp. 116-i 31, Clarendon Press 9 Dobson, F.S. and jones. WT. ( 19851 Am Nat. I26,855-858 IO Pusey, A.E. (19871 Trends Ecol. Evol 2, 295-299 I I Kieiman, D.C. CI9801 in Conservation Biology: An Evolutionary-Ecological Perspective ISoule, M.E. and Wilcox, B.A.. edsl, pp. 243-262, Sinauer Associates. Inc I2 Epple, G. and Katz. Y. ( I9841 Am. 1. Primatof. 6,2 15-227 13 Harcourt, A., Stewart, K., Fossey, D. ( 19761 Nature 263,226-227 I4 Armitage, K.B. ( I9841 in Biology of Ground-DwellingSquirrels IMurie, I.0 and Michener, CR, eds). pp. 377-403, University Nebraska Press I5 Koenig, W.D., Mumme, R.L. and Pitelka, F.A. ( 19841 Z. Tierpsychol. 65,289-308 I6 Hill, I.L. II9741 Science 186, 1042-1044 I7 Agren.G.(1984lBehavior91,229-243 18 McGuire, M.R. and Getz, L L. ( I98 I I 1.Mammal. 62,2 13-2 I 5 I9 Batzil, G.O., Getz. L.L. and Hurley. S.5 ( 19771 I. Mammal. 58,583-59 I 20 Dewsbury, D.A. ( 19821 Biol Behav. 7. 157-169 21 Packer, C. ( 19791 Anim. Behav. 27, I-36 22 Hanby, I.P. and Bygott. j.D ( I9871 Anim. Behav. 35, 161-169 23 Pusey, A.E. ( I9801 Anim. Behav 28. 543-552 24 Spiro, M.E. (19581 Children of the Kibbutz, Harvard University Press 25 Wolf, A.P. ( 19661 Am. Anthropof 6X. 885-898
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26 Wilson, E.O. 11978) On Human Nature, Harvard University Press 27 Knoppien. P. ( I9851 Biol. Rev. 60,8 l-1 I 7 28 Farr, J.A. ( 19801Behavior 74, 3&90 29 Lacy, R.C. ( I9791 Behav. Cenet. 9,5 l-54 30 Bruce, H M. I I960 I 1.Reprod. Fertil. I
Tkere is currently great concern over the po;si&le adverse effects of atmospheric deqosition and other regionally distributed po,lutants on plants and plant communitie;. In Europe and North America there arcs major research efforts to determine whether such pollutants damage plants or affect ecosystem processes. A topic of growinq concern is the possibility of genetic or evolutionary effects of pollutants. Past research has demonstrated that indivisuals, populations and varieties of a pa kular species can differ in their response to pollutants. Although such differwces have been documented, the im sortance of evolutionary responses to regional, low level but chronic pollution rervains to be established. The significance of vegional chronic pollution is that effects on plants may no longer 6e limited to heavily industrialized or populated areas, 6~’ rather may also occur in virtually all na ‘Ural ecosystems. rerrestrial plants have adapted to a wide range of natural conditions. There is no fundamental reason why plants should not adapt to stress resulting from human activities, especially if these are simply va;-iations on natural conditions. Plants are abundant on soils naturally deficient in essential minerals or with potentially toxic levels of certain elements’,2. They also occur around sulfur hot springs or other areas with naturally high levels of sulfur dioxide’. Hutchinson has commented that plants ‘. do not dil;,tinguish between natural and an,:hropogenic air pollution’. Other evidence also suggests that pollutants might be a signiflcant selective force affecting plants. For instance, the potential for populations of plant species to ad.spt to localized stress is well established. Such ecotypic differentiation has been documented in nany species and in response to Lobis Pitelka is at the Ecological Studies Program, Elel:tric Power Research Institute, P.0 Box 10412, Palo Alto, California 94301, USA.
96-103 II Stehn, R.A.and Richmond, M.E. (19751 Science 187, 121 l-1213 32 Shields, W.M. 11983) Philopatry, Inbreedingand the Evolution of Sex, Suny Press
33 Templeton, A.R. 11986) in Conservation Biology: The Science of Scarcity and DiversitylSoule. M., ed.), pp. 105-l 16, Sinauer Associates, Inc. 34 Waser. P.M., Austad, S.N and Keam, B. ( 19861AmNat. 128,529-537
EvolutionaryResponsesof Plantsto AnthripogenicPollutants Louis F, Pitelka many different kinds of stress. The potential for rapid evolutionary change in response to air pollution has been established for animals with the extensive studies of industrial melanism in Great Britain4. Occurrence of resistance I adopt the same definition of ‘resistance’ as that used by Roose et a1.5 and Baker’. Resistance is a quantitative trait which enables a plant to survive, grow and reproduce in the presence of a particular pollutant. It can involve either ‘tolerance’ or ‘avoidance’ of pollutant+. A considerable amount of research has been carried out on the occurrence in plants of resistance to anthropogenic soil and air pol-
Table
1. Examples
of recently
published
Pollutant Ozonea
lutants (Table 1I. The phenomenon of resistance to heavy metals in plants growing on soils either polluted with metals or having naturally high levels has been well studied and recently reviewed2823. Plant populations differ in their capacity to develop resistance to heavy metals, and these differences are due, at least in part, to the availability of appropriate genetic variation (Fig. 1124825 Populations possessing latent variability for resistance can usually evolve resistant populations if exposed to high concentrations of a metal. Populations lacking such variability cannot become resistant. Many instances of metal pollution of soils are associated with mining and smelting; because dates of initiation of these activities
reports documenting pollutants.
Life form Trees
intraspecific
Species
variation
in sensitivity to Reference
Populus tremuloides Pinus taeda Picea abies various crops
7 8 9 10
Picea abies various conifers Silene cucubalus various grasses
11 12 13 14
Trees Vines
Pinus silvestris Vitis vinifera
15 16
Dioxide
Herbs
Plantago
17
Heavy MetalsC
Trees Herbs
Betula spp. Agrostis capillaris Silene cucubalus Funaria h ygrometrica
HeYbs Sulfur
Dioxidea,b
Trees Herbs
Hydrogen
Carbon
Fluoride
Mosses
%ee Ref. 5 for more examples; examples.
lanceolata
bsee Ref. 21 for more examples;
18 19 13 20
Csee Ref. 22 for more
