Heterochrony in Tingidae (Insecta: Heteroptera):
paedomorphosis and/or peramorphosis?
ERIC GUILBERT*, LAURE DESUTTER-GRANDCOLAS and PHILIPPE GRANDCOLAS
UMR 5202 CNRS, Muséum National d’Histoire Naturelle, Département Systématique et Evolution,
CP50 - 45 rue Buffon, 75005 Paris, France
Received 24 November 2006; accepted for publication 19 March 2007
Tingidae (Heteroptera: Insecta) exhibit cephalic tubercles that present a very diverse shape in larvae but that are
much simpler in adults. A phylogeny based on adult and last instar characters showed that these tubercles evolved
independently from simple to complex states in two clades, and reversed from complex to simple in some taxa.
These homoplasies are analysed in the light of ontogenetic sequences and interpreted as heterochronic events. The
general trend of evolution of the cephalic tubercles in Tingidae is in mosaic, and could be generally peramorphic,
with some isolated cases of paedomorphosis. Journal compilation © 2008 The Linnean Society of London,
Biological Journal of the Linnean Society, 2008, 93, 71–80. No claim to original French government works.
ADDITIONAL KEYWORDS: Ontogenetic sequence – ontogenetic stage – ontogeny – phylogeny.
INTRODUCTION
Heterochrony is defined as a change in rate of
development that produces changes in morphology
between an immediate ancestor (i.e. an ancestral
morphotype in phylogeny) and its descendant(s). ‘It
could be a source of evolutionary innovations, includ-
ing homoplasy’ (Brooks & McLennan, 2002). Accord-
ing to DeBeerian classification (DeBeer, 1958; Raff &
Wray, 1989), and restricting heterochrony to what
Smith (2002) called ‘growth heterochrony’ (affecting
only size and shape) or to what Alberch et al. (1979)
called ‘allometric heterochrony’ (in opposition to het-
erochrony s.s., affecting age and shape), there are six
different cases of heterochronic phenomena leading to
two general categories of heterochronic expressions:
paedomorphosis and peramorphosis. Paedomorphosis
leads to a descendant with ‘underdeveloped’ character
states compared to its immediate ancestor; peramor-
phosis leads to a descendant with ‘overdeveloped’
character states compared to its immediate ancestor,
which implies a recapitulation sensu Agassiz
(1833–1843) of the ancestral ontogeny during devel-
opment (Futuyma, 1998).
Heterochrony has been widely studied in evolution
and developmental biology (the so-called ‘evo-devo’),
and has recently been a matter of most interest in a
phylogenetic frame. In a first approach, Gould (1977)
considered the different ways heterochrony has been
treated with regard to phylogeny. Alberch et al. (1979)
developed a general model describing heterochronic
changes of size and shape in the frame of phylogeny.
Fink (1982) replaced comparative analyses of ontog-
eny in the context of phylogenetic hypotheses to
explain homoplastic changes by heterochronic events:
paedomorphosis would then be characterized by a
reversal to the ancestral state in a phylogenetic
context, and recurring peramorphosis would produce
homoplasious changes, revealed by a parallelism
pattern (for terminology about convergence versus
parallelism, see Desutter-Grandcolas et al., 2005).
Steyer (2000) proposed a method based on a com-
parison between a total evidence approach (involving
all the available ontogenetic stages) and a systematic
congruence approach (involving a phylogeny for each
ontogenetic stage, represented by ‘ontotree’). The
‘event pairing’ or ‘sequence units’ method was pro-
posed to analyse sequence heterochrony in the frame *Corresponding author. E-mail: guilbert@mnhn.fr
Biological Journal of the Linnean Society, 2008, 93, 71–80. With 4 figures
Journal compilation © 2008 The Linnean Society of London
No claim to original French government works
, Biological Journal of the Linnean Society, 2008, 93, 71–80 71