Salamanders breeding in subterranean habitats:
local adaptations or behavioural plasticity?
R. Manenti
1
& G. F. Ficetola
2
1 Dipartimento di Bioscienze, Università degli Studi di Milano, Milano, Italy
2 DISAT, Università degli Studi di Milano – Bicocca. Milano, Italy
Keywords
cave; Salamandra salamandra; underground;
ecology; predation performance;
biospeleology.
Correspondence
Raoul Manenti, Diupartimento di Bioscienze,
Università degli Studi di Milano, Via Celoria,
26, Milano, 20133, Italy.
Email: raoul.manenti@unimi.it
Editor: Mark-Oliver Rödel
Received 14 May 2012; revised 14
September 2012; accepted 14 September
2012
doi:10.1111/j.1469-7998.2012.00976.x
Abstract
The exploitation of novel habitats requires the expression of specific behaviours.
This may occur through both behavioural plasticity and local adaptations, but
assessing the relative role of these processes is challenging. Animals colonizing
underground environments are exposed to strong selective pressure: epigeous
species using caves during one or more phases of their life cycles can help to
understand mechanisms allowing cave exploitation. The fire salamander (Sala-
mandra salamandra) may breed both in cave springs and in epigeous streams. We
compared predation performance of larvae from cave and stream populations,
and assessed whether local adaptations or behavioural plasticity (or both)
improve predation in underground environments. We performed a behavioural
experiment about prey detection and capture. We collected larvae from both caves
and streams, and reared them under contrasting conditions: underground and
outdoor. In the darkness, we tested two measures of predation performance of
larvae: time of head turning towards the prey and frequency of prey capturing. We
used an information-theoretic approach to assess the relative support of potential
mechanisms (adaptations vs. plasticity). Both cave and stream larvae were able to
detect and capture prey in the darkness. Larvae born in caves captured prey with
higher success than those from streams. Acclimatization to underground condi-
tions did not improve predation performance, suggesting that plasticity plays a
minor role. This study indicates that the exploitation of underground environ-
ments leads to behavioural local adaptations, allowing an improved predation
performance in environments where prey are both scarce and difficult to detect.
Introduction
During the exploitation of new habitats, populations are
exposed to selective pressures that may lead to evolutionary
adaptations for multiple traits, such as behaviour, morphol-
ogy, metabolism and physiological tolerance. Such intraspe-
cific adaptations can evolve quickly, particularly when natural
selection is strong, or generation time is fast (Miner et al.,
2005; Steinfartz, Weitere & Tautz, 2007). On the other hand, a
single genotype can generate multiple phenotypes in response
to variation of abiotic and biotic conditions of environments
(phenotypic plasticity; Miner et al., 2005; Gomez-Mestre,
Touchon & Warkentin, 2006). Phenotypic plasticity allows a
quick response to environmental conditions, may favour the
colonization of heterogeneous habitats (Hawlena, Hughes &
Schmitz, 2011; Peacor et al., 2011; Jourdan-Pineau, David &
Crochet, 2012) and can play an important role in adaptation
processes (Price et al., 2003). Although plasticity may absorb
the effects of environmental variation and reduce the genetic
response to selection, thus retarding evolutionary change
(Gomez-Mestre & Buchholz, 2006), it may facilitate evolu-
tionary diversification if environmentally induced phenotypic
changes allow populations to survive or colonize different or
new habitats, and thus develop independently evolving line-
ages (Gianoli & Valladares, 2011; Lind & Johansson, 2011).
When the new habitat strongly differs from the usual one,
the emerging adaptations are expected to be particularly
important (Dreiss, Guillaume & Clobert, 2009). Underground
environments are extremely interesting to understand the
processes allowing the exploitation of novel environments
(Jugovic et al., 2011; Riesch, Plath & Schlupp, 2011). Under-
ground environments differ from the epigeous ones for mul-
tiple features, such as light scarcity, limited food and stability
of microclimate (Culver et al., 2004). Epigeous species
attempting the colonization of underground habitats are
exposed to strong selective pressures that can induce dramatic
phenotypic changes, and may lead to genetic adaptations
favouring individual development, survival and fitness (Frie-
drich et al., 2011; Riesch et al., 2011). These changes can be
both morphological, such as in underground populations of
the fish Astyanax fasciatus that evolved typical troglomorphic
features (loss of eyes and pigmentation; Salin et al., 2010), and
Journal of Zoology
Journal of Zoology. Print ISSN 0952-8369
182 Journal of Zoology 289 (2013) 182–188 © 2013 The Authors. Journal of Zoology © 2013 The Zoological Society of London