The adaptive significance of the scrotum and the evolution of the descent o
f the testicles and epididymis have been a focus of interest among biologis
ts for a long time. In this paper we use three anatomical character states
of the scrotum and descensus: (1) testicles descended and scrotal; (2) test
icles descended but ascrotal; (3) testicles not descended (testicondy). The
se states are then mapped on an up to date phylogeny of the Mammalia. Three
main points arise out of this mapping procedure: (1) the presence of a scr
otum is either primitive in extant Mammalia or primitive within eutherian m
ammals except Insectivora; (2) evolution has generally proceeded from a scr
otal condition to progressively more ascrotal; (3) loss of testicular desce
nsus is less common in mammalian evolution than is loss of the scrotum. In
the light of these findings we discuss some current hypotheses regarding th
e origin and evolution of the scrotum. We find that these are all incomplet
e in so far as it is not the presence of the scrotum in various mammal grou
ps that requires explaining. Instead, it is the reverse process, why the sc
rotum has been lost in so many groups, that should be explained. We suggest
that the scrotum may have evolved before the origin of mammals, in concert
with the evolution of endothermy in the mammalian lineage, and that the sc
rotum has been lost in many groups because descensus in many respects is a
costly process that will be lost in mammal lineages as soon as an alternati
ve solution to the problem of the temperature sensitivity of spermatogenesi
s is available. (C) 1999 Academic Press.