The existence of species rests on a metastable equilibrium between inbreeding and outbreeding. An essay on the close relationship between speciation, inbreeding and recessive mutations

Abstract

Background: Speciation corresponds to the progressive establishment of reproductive barriers between groups of individuals derived from an ancestral stock. Since Darwin did not believe that reproductive barriers could be selected for, he proposed that most events of speciation would occur through a process of separation and divergence, and this point of view is still shared by most evolutionary biologists today.

Results: I do, however, contend that, if so much speciation occurs, the most likely explanation is that there must be conditions where reproductive barriers can be directly selected for. In other words, situations where it is advantageous for individuals to reproduce preferentially within a small group and reduce their breeding with the rest of the ancestral population. This leads me to propose a model whereby new species arise not by populations splitting into separate branches, but by small inbreeding groups "budding" from an ancestral stock. This would be driven by several advantages of inbreeding, and mainly by advantageous recessive phenotypes, which could only be retained in the context of inbreeding. Reproductive barriers would thus not arise as secondary consequences of divergent evolution in populations isolated from one another, but under the direct selective pressure of ancestral stocks. Many documented cases of speciation in natural populations appear to fit the model proposed, with more speciation occurring in populations with high inbreeding coefficients, and many recessive characters identified as central to the phenomenon of speciation, with these recessive mutations expected to be surrounded by patterns of limited genomic diversity.

Conclusions: Whilst adaptive evolution would correspond to gains of function that would, most of the time, be dominant, this type of speciation by budding would thus be driven by mutations resulting in the advantageous loss of certain functions since recessive mutations very often correspond to the inactivation of a gene. A very important further advantage of inbreeding is that it reduces the accumulation of recessive mutations in genomes. A consequence of the model proposed is that the existence of species would correspond to a metastable equilibrium between inbreeding and outbreeding, with excessive inbreeding promoting speciation, and excessive outbreeding resulting in irreversible accumulation of recessive mutations that could ultimately only lead to extinction.

Figure 1

Comparing the effects of accumulation of recessive deleterious mutations in populations undergoing various degrees of inbreeding, and with a theoretical completely outbred population. Panel A: Mendelian laws predict that when a crossing occurs between two individuals heterozygous for a recessive deleterious mutation, allelic frequency for that mutation drops from 0.5 in the parents to 0.33 in the offspring. Panel B: Evaluation of the fertility as a function of mutation loads and inbreeding coefficients. The thick red curve corresponds to the fertility predicted in a completely outbred population. It was drawn with the equation F = (1- M².10^-8)^10,000 (see text). The thinner curves of different colours correspond to the fertility of crosses with a certain degree of inbreeding, as indicated on the figure. Those were calculated as F = (1- I)^M, where F is the predicted fertility, M the average mutation load in the population, and I the inbreeding coefficient. In natural populations, the actual fertility would be a factor of those two theoretical degrees of fertility.

Figure 2

Predicted chromosomal structures in zygotes issued from individuals carrying a whole arm reciprocal chromosomal translocation. In an individual carrying a reciprocal chromosomal translocation, only 50% of the offspring is viable (first line). If the cross takes place between two heterozygotes, the proportion of viable offspring drops to 6/16 (= 3/8). Once the translocation has become fixed in a population, crosses with the ancestral stock will generate a first generation (F1) that will be 100% viable, but those F1 individuals will be back to the situation of reduced fertility faced by the individuals who first carried the translocation, and this will be true whether they cross to individuals from the ancestral stock, or to individuals homozygous for the translocation.

Figure 3

Schematic representation of the three major modes of speciation.

Figure 4

The existence of species rests on a metastable equilibrium between inbreeding and outbreeding.