Trait independence primes convergent
Molly C. Womack,
Tyler S. Fiero,
and Kim L. Hoke
Department of Biology, Colorado State University, Fort Collins, Colorado 80523
Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, District of
Received November 30, 2017
Accepted January 21, 2018
The repeated, independent evolution of traits (convergent evolution) is often attributed to shared environmental selection pres-
sures. However, developmental dependencies among traits can limit the phenotypic variation available to selection and bias
evolutionary outcomes. Here, we determine how changes in developmentally correlated traits may impact convergent loss of the
tympanic middle ear, a highly labile trait within toads that currently lack adaptive explanation. The middle ear’s lability could
reﬂect evolutionary trade-offs with other skull features under selection, or the middle ear may evolve independently of the rest
of the skull, allowing it to be modiﬁed by active or passive processes without pleiotropic trade-offs with other skull features. We
compare the skulls of 55 species (39 eared, 16 earless) within the family Bufonidae, spanning six hypothesized independent middle
ear transitions. We test whether shared or lineage-speciﬁc changes in skull shape distinguish earless species from eared species
and whether earless skulls lack other late-forming skull bones. We ﬁnd no evidence for pleiotropic trade-offs between the middle
ear and other skull structures. Instead, middle ear loss in anurans may provide a rare example of developmental independence
contributing to evolutionary lability of a sensory system.
Bufonidae, developmental bias, pleiotropy, tympanic middle ear, Williston’s law.
The repeated, independent evolution of traits (convergent evolu-
tion) is often attributed to shared environmental selection pres-
uber and Adams 2001; Harmon et al. 2005; Rosenblum
2005; Edwards et al. 2012; McCurry et al. 2017). However, devel-
opmental dependencies among traits can contribute to convergent
evolution by limiting the phenotypic variation available to selec-
tion (Arthur 2002; Beldade et al. 2002; Kavanagh et al. 2013).
Thus, developmental factors can bias evolutionary lability and
may help explain convergent traits that lack adaptive explanation.
For example, convergent eye loss in cavefish, once ascribed to
a combination of relaxed selection pressures and high energetic
cost, is now attributed to selection for enhanced taste buds that
are genetically linked to eye reduction (Yamamoto et al. 2009).
Thus, trait lability can result from genetic and/or developmental
links among traits (trait integration) that cause traits to change in
concert (Wright 1964, 1980; Mayr 1976; Kavanagh et al. 2013).
On the other hand, traits capable of evolving independently of
other traits are freed from pleiotropic trade-offs and may be more
flexible (Beldade et al. 2002; Esteve-Altava et al. 2014). Here, we
investigate whether convergent loss of the tympanic middle ear in
anurans, which currently lacks adaptive explanation, is associated
with changes in other skull features or whether the middle ear
shows evolutionary independence with respect to developmen-
tally linked skull features.
Most tetrapods have a tympanic middle ear, which functions
to transmit airborne sound from the environment to the inner ear
sensory hair cells (reviewed in Manley 2010). The anuran middle
ear functions similarly to those found in other tetrapods and con-
sists of numerous structures: a tympanic membrane surrounded
by a cartilaginous tympanic annulus, a mostly bony middle ear
column, and a middle ear cavity connected to the buccal cavity via
the Eustachian tube (Lewis and Narins 1999). In species that have
lost their tympanic middle ears, a condition termed earlessness,
the inner ear remains but all middle ear structures are missing
2018 The Author(s). Evolution
2018 The Society for the Study of Evolution.
Evolution 72-3: 679–687