The Natural History of Inbreeding and Outbreeding.
To my knowledge, The Natural History of In-breeding and Outbreeding is the first full-length volume since Darwin to be devoted to the general evolutionary problems presented by the evolution of outbreeding versus inbreeding. It naturally raises the question of how much progress has been made in the last 117 years. Readers of this book might come away feeling that the answer is: not much! This is, I hope, a somewhat misleading impression, due in large measure to the book's emphasis on studies of natural or captive animal populations (11 of 18 chapters are in part or wholly devoted to such studies). Our advances since Darwin have come about on three fronts, all rather removed from this topic. The first is an improved, although still incomplete, understanding of the genetic basis of inbreeding depression. We now know that the decline in mean of component of fitness caused by inbreeding is mainly a result of homozygosity either for alleles at loci subject to selection favoring heterozygotes, or for recessive or partially recessive alleles maintained by mutation-selection balance. There is still room for debate on the relative importance of these factors, although the consensus tends to favor the mutational hypothesis. This debate is only touched on a few times here. Jeffrey Mitton argues strongly that observed associations between degree of heterozygosity for electrophoretic loci and fitness imply a direct causal relation. He downplays the possibility that most cases of such association are artifacts of an association between heterozygosity at the loci under study, and the general level of heterozygosity in the genome, generated by variation between individuals in their level of inbreeding. I did not find his arguments convincing as establishing the universal importance of heterozygote advantage, although no doubt there are individual cases where it clearly plays a role. In particular, he ignores the study of Pinus attenuata by Stephen Strauss (1986), which experimentally demonstrated that removal of variation in level of inbreeding removes most of an observed association between heterozygosity and fitness.
At the other extreme, John Werren presents an admirably clear theoretical investigation of the effects of inbreeding in haplodiploid organisms, on the assumption that inbreeding depression is largely mutational in origin. Unfortunately, there is no chapter reviewing the information derived from experimental genetic studies of diploid organisms, so that the reader of this volume is left to go to the literature for much relevant information. The wealth of information from studies of viability in Drosophila is barely mentioned (there are only six reference to D. melanogaster in the index). Many salient facts from the Drosophila work, such as that half the genetic load revealed by inbreeding is due to genes of minor effect which are only partially recessive in their effects on fitness, are mentioned only by Werren. As noted by Werren and by Donald Waller, even lethal alleles tend to have measurable effects on the fitness of their heterozygous carriers, but several other authors persist in stating that detrimental alleles are recessive. No reference is made to the monumental work of Terumi Mukai on estimating the rate of mutation per genome to deleterious alleles in D. melanogaster, a parameter of crucial importance for the interpretation of inbreeding depression.
The reason for this neglect of the genetics literature seems to be the feeling on the part of several contributors that laboratory data are not good guides to what happens in nature. This view is particularly strongly stated by Williams Shield in chapter 8, who alludes to "the dogma that inbreeding depression is harmful". He relies on the conflicting evidence from studies of relatively small studies of natural populations of animals to argue that "In the vertebrates, in every case with sufficient evidence there is either no inbreeding depression or in a few cases even significant depression enhancement." To a geneticist, this failure to acknowledge that the results of dozens of careful laboratory studies of organisms should be weighed against much smaller studies conducted under less controlled conditions seems extremely foolish, particularly when a number of recent studies of plants have documented inbreeding depression under natural conditions. It is analogous to someone suggesting that Mendelian genetics is unproven for deep-sea fishes, because no one has demonstrated 3:1 ratios at a depth of 2 miles. Given the evidence for a major role of deleterious mutations in contributing to inbreeding depression in Drosophila and some plants, it seems inconceivable that vertebrates, with their much larger genomes, could in some magical way escape from it. Indeed, a large effect of inbreeding is exactly what the laboratory data show for mice, guinea pigs, Japanese quail, etc. In contrast to Shields, Bruce Waldman and Jeffrey McKinnon cite evidence for inbreeding depression in lower vertebrates; Robert Lacy, Ann Petric, and Mark Warneke carefully review evidence for inbreeding depression in captive populations of wild animals; and Craig Packer and Ann Pusey provide circumstantial evidence for inbreeding depression in lions.
This leads to the second topic that is not adequately covered: the theoretical evolutionary genetics of inbreeding and outbreeding. Despite lengthy contributions by leading theorists such as Richard Michod, Marcy Uyenoyama, and Werren, the book does not provide a comprehensive overview of the current state of knowledge for the reader who is not already familiar with the literature. Readers are largely left ignorant of the recently developed methods for studying multilocus systems subject to mutation-selection balance that have already been used to model the evolution of genetic modifiers of the breeding system. Theoretical analyses based on these methods have shown that the effect of continued inbreeding in "purging" deleterious alleles from the population, and hence reducing the magnitude of inbreeding depression, is much smaller when alleles are partially recessive than when they are completely recessive. This implies that populations that have come to equilibrium under high levels of close inbreeding may still retain significant levels of heterosis, as measured by the contrast in fitness between experimental outcrosses and inbred matings. Ironically, this is associated with an increase in equilibrium population mean fitness compared with the random-mating case, which does not occur when deleterious mutations are recessive. The question of the extent to which a short-term loss in fitness as a result of inbreeding depression can be offset by a subsequent gain in fitness as a result of purging is clearly as great importance both for conservation biologists interested in the maintenance of small populations, and for an understanding of natural mating systems. However, the relevant results in the recent literature are only touched on briefly in this volume, in the chapters by Waller and by Werren.
Third, the book does not draw together a coherent picture of the evolutionary forces modulating levels of inbreeding and outbreeding. This makes it hard to assess the current status of the experimental and comparative evidence concerning their importance, despite the wealth of information provided on individual systems. Only Nancy Knowlton and Jeremy Jackson's survey of marine invertebrates attempts to review comparative data on patterns relating the level of close inbreeding to ecological factors. This reviewer is left, for example, with a sense of uncertainty as to whether there really is good evidence to support the role of reproductive assurance in promoting close inbreeding in marginal habitats, as suggested in the third quotation from Darwin. This in part reflects the very different concepts among the authors of what counts as inbreeding, and the identification by many of them of finite population size and population subdivision with inbreeding (e.g., Nikolas Waser, chap 1; Daniel Howard, chap. 7).
Although there is a technical justification for using the term inbreeding in this context, the evolutionary problem posed by Darwin clearly involves the question of how adaptations are evolved either to promote or to prevent a specific class of matings (self-fertilization). Confusion is bound to be created by lumping this question, and the analogous problem of the evolution of the frequency of matings among close kin when sexes are separate, with the much more complex issue of how migration patterns and population structure are determined. Thus, several chapters (especially Waser's chap. 9) discuss the concept of "outbreeding depression" as a factor in promoting the evolution of an intermediate level of inbreeding. There is no doubt that crosses between different species usually produce severe fitness losses to the hybrids, that lesser effects are sometimes found for hybrids between different geographic races, and that more minor but significant effects can be detected in crosses over relatively short ranges in some populations, presumably as a result of genetic differences that have evolved in response to local selective conditions. But these observations are of doubtful relevance to the question of the existence of an intermediate optimum rate of close inbreeding within a local population, and it seems that the use of the term "optimal outbreeding" by Waser is not really intended to imply that this is the case. In addition, there is no good chapter on how such outbreeding depression can evolve; the chapter by Howard on speciation is seriously flawed by a whole-hearted acceptance of the genetic revolution school of thought and a failure to cite any of the literature that is critical of it.
This book has the virtue of containing a massive amount of information, especially on the breeding structure of natural populations, and will no doubt provide a very useful resource for many years to come. Many of the individual articles are lucid and informative, although some are not. But the book as a whole fails to present a coherent theme, and overall does not do justice to its subject. Darwin still reigns supreme.
Darwin, C. R. 1876. The effects of cross and self fertilisation in the vegetable kingdom. J. Murray, London.
Strauss, S. H. 1986. Heterosis at allozyme loci under inbreeding and crossbreeding in Pinus attenuatus. Genetics 113:115-134.