Fire-adapted traits in animals

Abstract

Fire is a pervasive driver of trait evolution in animals and its importance may be magnified as fire regimes rapidly change in the coming decades. This was the thesis of our paper published recently in Trends in Ecology and Evolution [1]. In their response letter, Nimmo et al. [2] reinforce our thesis and suggest expansion of some of our conceptual models.

Full text

Letter
Fire-adapted traits in
animals
Gavin M. Jones ,
1,
*
Joshua F. Goldberg,
1
Taylor M. Wilcox,
2
Lauren B. Buckley,
3
Catherine L. Parr,
4,5,6
Ethan B. Linck,
7
Emily D. Fountain,
8
and
Michael K. Schwartz
2
Fire is a pervasive driver of trait evolution
in animals and its importance may be
magnified as fire regimes rapidly change
in the coming decades. This was the
thesis of our paper published recently in
Trends in Ecology and Evolution [1]. In
their response letter, Nimmo et al.[2] rein-
force our thesis and suggest expansion of
some of our conceptual models.
Specifically, Nimmo et al.[2] outline two
possible additions. First, they argue that
a broader range of traits should be con-
sidered as potentially being responsive
to fire and draw particular attention to
reproductive and phenological traits. This
expanded range of traits is likely to expe-
rience selective pressure in response to
different axes of a fire regime, for exam-
ple, selection on breeding strategies
may be closely linked to fire seasonality.
Second, Nimmo et al.[2] suggest an ex-
pansion of the definition of ‘fire-adapted’
fauna to include a broader swath of taxa
that may not have obvious traits to facili-
tate fire survival or persistence, but in-
stead may have evolved movement or
dispersal strategies that enhance their
persistence in fire-prone landscapes.
Traits can be difficult to characterize
since they aggregate in complex ways
to determine organismal performance
in dynamic environments, particularly
fire-prone environments. We agree some
expansion is beneficial beyond the
categories we included: behavioral, physio-
logical, and morphological traits, which
were originally proposed by Pausas and
Parr [3](Figure 1). Yet many traits related
to phenology and reproduction fall within
existing categories. Both phenology and
reproduction are often set by developmen-
tal rates and other physiological traits, and
sometimes phenological and reproductive
traits involve behavioral responses to envi-
ronmental cues related to the seasonal
timing of events. One productive strategy
aligned with what Nimmo et al.[2]suggest
is to consider fire-driven life history evolu-
tion, which relates to pace-of-life syn-
dromes, age-dependent strategies, juvenile
development, lifespan, and similar traits. A
comprehensive consideration of linkages
between fire and life history can illuminate
evolutionary responses to fire [4].
We appreciate the emphasis by Nimmo
et al.[2] on animal movement strategies
and we agree they should be considered
fire-adapted traits. Fire-associated move-
ment and dispersal strategies may repre-
sent a promising avenue for future fire-
driven evolution research given they are
relatively easy to study, for example, using
GPS or satellite transmitters. The potential
evolutionary importance of movement
strategies was noted by Pausas and Parr
[3], where they give ‘ability to move long-
distance’as an example of a trait that
Behavioral | Habitat selection
Survival of juvenile black-backed
woodpeckers (Picoides arcticus) is
higher when nests (in fire-killed
trees) are in closer proximity to
‘green’ forests. Such nest site
selection behavior would be
reinforced through evolutionary
change if it is genetically based and
thus heritable.
Fire regime axis: severity
Behavioral | Dispersal strategy
Queen yellow-faced bumble bees
(Bombus vosnesenskii) have been
shown to disperse up to 8km,
leading to a ‘spillover’ effect of
increased abundance of queens in
unburned areas. Long-distance
dispersal may thus be a fire-adapted
trait that facilitates metapopulation
persistence.
Fire regime axis: scale
Morphological | Coat color
Eastern fox squirrels (Sciurus niger)
show variation in pelage across their
geographic range. Certain
intermediate coat colors are more
closely associated with
heterogeneous environments
produced by fire, which could
facilitate survival through
background color matching.
Fire regime axis: patchiness
Physiological | Immune function
California sea otters (Enhydra lutris)
were shown to have reduced
immune function following a large
wildfire because of exposure to
environmental contaminants,
exposing them to pathogens.
Variation in immune response
influencing fitness could lead to
rapid evolution in immunity.
Fire regime axis: scale, intensity
Life history | Phenology
Tree regeneration failure after fire
leads to warmer soil temperatures in
southwestern US riparian forests
that, in turn, can cause earlier
emergence dates for cicadas
(Tibicen dealbatus). Early
emergence could drive life history
evolution cicada-dependent species
at higher trophic levels.
Fire regime axis: seasonality
Life history | Reproduction
Following wildfire, reproductive
output declines for female Savi's
pipistrelle (Hypsugo savii) bats,
potentially to maximize overall
fitness by increasing the offspring
survival rates. Evolution of bet-
hedging reproductive strategies may
be expected in changing fire
regimes.
Fire regime axis: frequency
Nick Bossenbroek
J. Kehoe
Peter Richman
David Ledig/BLM
Dick Thompson
Tommy Andriollo
Trends
Trends
in
in
Ecology
Ecology &
Evolution
Evolution
Figure 1. Examples of potential fire-driven trait evolution in animals and possible fire regime axis that
may drive selection. We identify four classes of traits: behavioral, morphological, physiological, and life history
traits, indicated by different box colors. Note that we have included ‘dispersal strategy’as a type of behavioral
trait and ‘phenology’and ‘reproduction’as types of life history traits. From upper left to lower right, the studies
corresponding with the examples are Stillman et al.[7](topleft),Molaet al.[8] (top right), Potash et al.[9]
(middle left), Bowen et al.[10] (middle right), Smith et al.[11] (bottom left), Ancillotto et al.[12] (bottom right). All
photos are used under a CC-BY license or are in the public domain.
Trends in Ecology & Evolution, Month 2023, Vol. xx, No. xx 1
Trends in
Ecology & Evolution
TREE 3226 No. of Pages 2

could be adaptive for animals living in fire-
prone landscapes. Similarly, in our paper,
we wrote: ‘Whether fire facilitates or in-
hibits gene flow likely depends on the
scale of the fire relative to animal dispersal
capabilities…’ and ‘If the trait(s) related to
fire are heritable, vary within the population,
and create a fitness differential (i.e., different
phenotypes show variance in survival),
selection will act upon the distribution of
trait values within a population’. Thus, we
think that fire-adapted fauna should be
defined as those with any type of genetically
based traits that increase the fitness of
animal populations in response to fire
regimes, which could include movement,
dispersal, life-history strategies, and any
others.
We concur with the need for a broad view
of traits subject to selection. Responses to
novel selection pressures associated with
changed fire regimes will involve many
traits, even beyond those that have so far
been proposed by us and by Nimmo
et al.[2] (e.g., Figure 1). Combinations of
traits may be selected for that are novel
across evolutionary history [5]. Evolution
can be slowed substantially when novel
selection acts against existing trait correla-
tions [6]. Thus, we must think broadly and
synthetically about the many types of traits
mediating ecological and evolutionary
responses to fire in a changing world,
how they may interact, and to which com-
ponents of fire regime they may be linked
(Figure 1).Atthesametime,weneed
researchers to add case studies to under-
stand how selection of multiple traits actually
unfolds in laboratory and natural systems.
Our hope is that, like Nimmo et al.[2], more
researchers will attempt to downscale
and adapt the broad recommendations
we made in our paper to meet their needs
and their deep understanding of the sys-
tems they work on. We did not intend our
brieflistofthetypesoftraits(morphological,
behavioral, physiological) to be exhaustive
or all-encompassing and we suspect there
are classes of traits still not included after
our dialogue with Nimmo et al.[2].
Declaration of interests
No interests are declared.
1
USDA Forest Service, Rocky Mountain Research Station,
Albuquerque, NM 87102, USA
2
National Genomics Center for Fish and Wildlife Conservation,
USDA Forest Service, Rocky Mountain Research Station,
Missoula, MT 59801, USA
3
Department of Biology, University of Washington, Seattle, WA
98195, USA
4
Department of Earth, Ocean, and Ecological Sciences,
University of Liverpool, Liverpool, L3 5TR, UK
5
Department of Zoology and Entomology, Universityof Pretoria,
Hatfield 0028, South Africa
6
School of Animal, Plant, and Environmental Sciences,
University of the Witwatersrand, Wits 2050, South Africa
7
Department of Ecology, Montana State University, Bozeman,
MT 59717, USA
8
Department of Forest and Wildlife Ecology, University of
Wisconsin, Madison, WI 53706, USA
*Correspondence:
gavin.jones@usda.gov (G.M. Jones).
https://doi.org/10.1016/j.tree.2023.09.016
Published by Elsevier Ltd.
References
1. Jones, G.M. et al. (2023) Fire-driven animal evolution in the
Pyrocene. Trends Ecol. Evol. Published online July 19,
2023. https://doi.org/10.1016/j.tree.2023.06.003
2. Nimmo, D.G. et al. (2023) Expanding the scope of fire-
driven animal evolution. Trends Ecol. Evol. Published online
September 26, 2023. https://doi.org/10.1016/j.tree.2023.
09.005
3. Pausas,J.G.andParr,C.L.(2018)Towardsanunder-
standing of the evolutionary role of fire in animals. Evol.
Ecol. 32, 113–125
4. Koltz, A.M. et al. (2018) Global change and the importance
of fire for the ecology and evolution of insects. Curr. Opin.
Insect Sci. 29, 110–116
5. Anderson,J.T.andSong,B.H.(2020)Plantadaptation
to climate change—where are we? J. Syst. Evol. 58,
533–545
6. Etterson, J.R. and Shaw, R.G. (2001) Constraint to adaptive
evolution in response to gl obal warming. Science 294 ,
151–154
7. Stillman, A.N. et al. (2021) Juvenile survival of a burned for-
est specialist in response to variation in fire characteristics.
J. Anim. Ecol. 90, 1317–1327
8. Mola, J.M. et al. (2020) Wildfire reveals transient changes to
individualtraits and populationresponses of a native bumble
bee Bombus vosnesenskii.J. Anim. Ecol. 89, 1799–1810
9. Potash, A.D. et al. (2020) Ecological drivers of eastern
fox squirrel pelage polymorphism. Front. Ecol. Evol. 8,
1–9
10. Bowen, L. et al. (2015) Effects of wildfire on sea otter
(Enhydra lutris) gene transcript profiles. Mar. Mammal Sci.
31, 191–210
11. Smith, D.M.et al. (2006) Cicada emergence in southwestern
riparianforest: influences ofwildfire and vegetationcomposi-
tion. Ecol. Appl. 16, 1608–1618
12. Ancillotto, L. et al. (2020) Resilient responses by bats to a
severe wildfire: conservation implications. Anim. Conserv.
24, 470–481
Trends in Ecology & Evolution
2Trends in Ecology & Evolution, Month 2023, Vol. xx, No. xx