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LETTER
Macroevolutionary consequences of
“spatial sorting”
In PNAS, Shine et al. (1) discussed the empirical evidence for,
and evolutionary importance of, “spatial sorting,” where reproduction between fast-dispersing individuals at a rangeexpansion front generates novel phenotypes, even in the absence
of conventional natural selection. Here, I suggest why the
process might be both less and more important than proposed,
and a likely key role for natural selection.
Species’ ranges cannot expand indefinitely: the exaggeration
of dispersal traits at the expansion front caused by spatial
sorting will eventually disappear, being gradually diluted after
range expansion ceases. If the lattice model were performed for
sufficient generations, equilibrium would probably be reached,
where the phenotypic frequencies throughout the entire area
would revert to initial values. The rowing race metaphor (where
nearby boats exchange rowers) illustrates the same point. The
overall numbers of good and poor rowers never change; it is
only their distribution across boats that is temporarily altered.
If the race is prolonged indefinitely so that the boats ply back
and forth across the lake, good and poor rowers will eventually
again be randomly distributed across boats. Thus, spatial
sorting by itself produces only a transient spatially structured
increase in phenotypic and genotypic variances (but not
means). Whether or not it has lasting importance depends on
other factors.
Spatial sorting will have more permanent (macro)evolutionary
effects if barriers hindering dispersal help maintain the integrity of the novel populations, and several of the proposed
examples (e.g., island birds, humans) involve such phenomena.
Although the importance of peripatric founder events for speciation has long been recognized (2), spatial sorting adds
a new facet to this process. Individuals comprising founder
populations could be deterministically biased according to
particular traits (dispersal filtering), which, in turn, would
accelerate phenotypic divergence and speciation.
www.pnas.org/cgi/doi/10.1073/pnas.1105702108
However, even in the absence of barriers, spatial sorting could
generate lasting effects despite its transient nature. First, it
represents an unusual example of “assortative mating by group
formation,” which favors the evolution of true assortative mating
(3). Second, natural selection interacting with spatial sorting
would lead to permanent changes. To emphasize the novelty of
the concept, Shine et al. (1) focused on how spatial sorting
can operate in the total absence of natural selection. However,
spatial sorting, by definition, applies to traits that are either
highly functional or linked to such traits, and it is unlikely that
such traits are neutral (or even “nearly neutral”). The empirical
examples included many of traits that have been demonstrated
to be highly adaptive and/or often used as proxies of “fitness,”
such as wing size, locomotor performance, and muscle mass (e.g.,
4). Spatial sorting will temporarily increase the species’ variance
of such traits, making new phenotypes “visible” to natural
selection; for example, polygenic traits will have greater variance
and extremes across the species, and harmful recessive alleles
that are associated with dispersal enhancement will be more
frequently homozygous (and thus expressed) at the advancing
edge. This is consistent with the high proportions of deformed
individuals at invasion fronts, although other factors could
generate these effects (5).
ACKNOWLEDGMENTS. This work is supported by the Australian
Research Council.
Michael S. Y. Lee1
School of Earth and Environmental Sciences, University of Adelaide, SA 5005, Adelaide, Australia; and Earth Sciences Section,
South Australian Museum, North Terrace, Adelaide 5000, Australia
1. Shine R, Brown GP, Phillips BL (2011) An evolutionary process that assembles phenotypes through space rather than through time. Proc Natl Acad Sci USA 108:5708–5711.
2. Coyne JA, Orr HA (2004) Speciation (Sinauer, Sunderland, MA).
3. Otto SP, Servedio MR, Nuismer SL (2008) Frequency-dependent selection and the
evolution of assortative mating. Genetics 179:2091–2112.
4. Irschick DJ (2003) Measuring performance in nature: Implications for studies of fitness
within populations. Integr Comp Biol 43:396–407.
5. Brown GP, Shilton C, Phillips BL, Shine R (2007) Invasion, stress, and spinal arthritis in
cane toads. Proc Natl Acad Sci USA 104:17698–17700.
Author contributions: M.S.Y.L. performed research and wrote the paper.
The author declares no conflict of interest.
1
E-mail: [email protected].
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