  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.
