One goal when I began research on crossbills was to figure out what seasons
or resources were the most critical in the evolution of trophic structure. What
characterizes the periods or resources that animals are adapted to exploit?
Similarly, when should we focus our studies if we are to understand community
structure? These were critical questions that were rarely addressed satisfactorily
and they remain important questions in ecology and evolutionary biology. Based
on prior field observations and laboratory experiments, I came up with three
characteristics of resources necessary for crossbills to specialize and then
quantitatively tested this hypothesis with captive representatives of four putative
species of Red Crossbill (L. curvirostra complex).
I
measured their feeding performances on cones that I hypothesized each species
was adapted to exploit given the cone characteristics as in the forestry literature.
[Here's a VIDEO that shows two call types foraging on western hemlock (Tsuga heterophylla) cones. The first birds are the small-billed call type 3, which are specialized for foraging on hemlock, whereas the last crossbill in the video is a much larger billed crossbill, call type 2. Nearly every time they lift their heads they are husking seeds. It is easy to see that the smaller billed call type is a much faster forager on hemlock cones.] The results were remarkable (Benkman
1993, Benkman and Miller
1996, Benkman et al.
2001). Each of the four taxa of crossbills had either an average
bill size (depth) or groove width in their palate where seeds are held, or both,
that approximated the predicted optima for foraging on the respective conifers.
This indicates that certain characteristics of resources are critical for specialization
- not only for crossbills but also for other predators (Thompson, J. N. 1994,
The Coevolutionary Process, Univ. Chicago Press).
I extended this work by converting estimates
of performance into fitness based on the relationships between morphology and
performance in captivity and between morphology and survival in the wild (Benkman
2003). The result was an extremely rugged adaptive surface, which implies
that divergent selection for foraging on different resources crossbills specialize
upon is driving the adaptive radiation of crossbills (PDF
of write-up in Science).
This
result is of substantial interest for two reasons. First, it provides the only
empirically derived three-dimensional adaptive surface for any group of organisms
that provides critical insight into an adaptive radiation. Adaptive surfaces,
first developed by Sewall Wright in 1932, are considered the most heuristically
valuable diagrams in all of evolutionary biology (Provine 1986:316) and
have been central to virtually all discussions of ecological speciation and
adaptive radiation because they capture how natural selection contributes to
population divergence, adaptive radiations and ultimately speciation. However,
adaptive surfaces are extremely difficult to quantify in a meaningful manner.
Second,
it is the first study that links measures of performance to fitness in the wild
and ultimately evolution. This linkage is central to theoretical arguments that
performance can be equated to fitness and to our understanding of adaptations.
Evolutionary biologists have devoted considerable effort trying to understand
coevolutionary arms races and how they contribute to biodiversity. Despite this
interest, few studies have demonstrated both reciprocal selection and reciprocal
adaptations for coevolving systems in the wild. We recently (Benkman
et al. 2003) provided empirical evidence demonstrating the forms of reciprocal
selection between two predators and their prey, and, in turn, how this results
in the evolution of reciprocal adaptations. Earlier (Benkman
1999, Benkman et al.
2001) we presented various lines of evidence that in sum demonstrate replicated
reciprocal adaptations between crossbills and lodgepole pine.
Red Crossbills are the principal seed predator and selective agent on Rocky
Mountain lodgepole pine (Pinus contorta ssp. latifolia) cones
in several isolated mountain ranges lacking red squirrels (Tamiasciurus hudsonicus).
In these ranges, crossbills have experienced selection favoring larger bills
and have coevolved in response to increases in structural seed cone defenses.
In contrast, where red squirrels are present, squirrels are the main selective
agent on seed defenses and cones evolve quite differently. The result is the
evolutionary divergence of crossbill populations in response to selection for
foraging on the different cones in areas with and without squirrels. This divergence
between crossbill populations is possibly leading to a new bird species in an
isolated range in Idaho (we collected the type specimens, which eventually we
will formally describe). Few studies have been able to capture and thoroughly
explain the forms of selection on the traits mediating and responding to selection
in a coevolutionary arms race. Even fewer studies can directly link the interaction
to the formation of new species. Speciation as the result of coevolution is
the subject of one of our two main avenues of future research.

South Hills, Idaho where crossbills are coevolving with lodgepole pine.
One of the central problems in evolutionary biology is to understand the processes
that lead to new species. Our currently NSF-funded research will determine whether
and how the coevolutionary arms race between Red Crossbills and lodgepole pine
is leading to what appears to be a new species of Red Crossbill. First, we are
using mark-recapture methods to determine whether natural selection because
of coevolution has caused the observed morphological divergence between crossbill
populations. Second, field studies and aviary experiments conducted by several
graduate students, Julie Smith
and Lisa Snowberg, are
addressing how reproductive isolation (i.e., speciation) might have occurred
as a by-product of divergent selection. Finally, one of my graduate students,
Thomas Parchman, is using AFLP (Amplified Fragment Length
Polymorphism) primers to determine the extent of genetic differentiation between
different crossbill populations and to develop a phylogeny of nearly all New
World crossbills. This work aims to link two of the most important evolutionary
processes, namely coevolutionary arms races and speciation, to patterns of biodiversity
and to how geographic patterns of diversity arise. The coevolutionary interactions
that have been documented, with the real possibility that they are contributing
to the origin of new species, is exciting and of fundamental importance yet
has rarely been as well documented for any taxa let alone for birds.
A second focus of our research is to determine the extent to which coevolution
between crossbills and conifers has contributed to the adaptive radiation of
crossbills. A fundamental challenge of evolutionary biology is to understand
the extent to which microevolutionary processes generate macroevolutionary patterns.
One of the most prominent hypotheses to explain macroevolutionary patterns is
that of a coevolutionary arms race between predators and their prey and other
exploiter-victim relationships. Although the details differ between authors,
antagonistic evolutionary interactions are thought to be responsible for patterns
of diversification of many taxa. Nevertheless, the extent to which coevolution
has played a role in the adaptive radiation of any group has not been well quantified.
Our previous research has
provided strong evidence of coevolution between Red Crossbills and both lodgepole
pine and black spruce (Picea mariana). What is further remarkable is
that the form of coevolution between crossbills and lodgepole pine is replicated
between crossbills and black spruce.Together these studies show that the presence
and absence of a dominant preemptive competitor, red squirrels, determines the
geographic selection mosaic and location of coevolutionary hotspots and coldspots
for its competitor, the Red Crossbill. Moreover, the patterns of cone evolution
in response to selection by crossbills and squirrels are repeated among populations
of lodgepole pine, and between lodgepole pine and black spruce (Parchman
and Benkman 2002), which enables predictions of coevolution in other systems.
Although
our understanding of the geographic mosaic of coevolution for crossbills that
specialize on lodgepole pine and black spruce is excellent, these findings might
not be general to other crossbills specialized on other conifers in North America
(and the Old World). There are two reasons to suspect this. First, annual fluctuations
in the availability of lodgepole pine and black spruce seed are much less variable
and not representative of most conifers; greater variation in the annual availability
of seed should limit the competitive and evolutionary impacts of territorial
or at least relatively sedentary tree squirrels. Second, Sciurus rather
than Tamiasciurus is the tree squirrel that more commonly co-occurs with
crossbills, and Sciurus is a weaker competitor than Tamiasciurus
because it harvests fewer cones.
Consequently, the main objectives of our study, recently funded by NSF, will
be to test two hypotheses. First, whether crossbills coevolve with conifers
whose seed availability fluctuates yearly. Second, whether the presence of tree
squirrels (Tamiasciurus or Sciurus) does not impede coevolution
between crossbills and conifers whose availability of seeds fluctuate. The results
of these studies will determine (1) how resource characteristics and competitor
type affect the form of the geographic mosaic for crossbills and conifers and
(2) to what extent coevolution has contributed to the adaptive radiation of
crossbills.