Diversifying Coevolution between Crossbills and Conifers
© Springer Science+Business Media, LLC 2009
Published: 16 December 2009
Coevolution between granivorous crossbills (Loxia spp.) and conifers has been a prominent process in the diversification of crossbills. A striking example occurs in western North America where coevolution between crossbills and Rocky Mountain lodgepole pine (Pinus contorta latifolia) is ongoing in isolated ranges without the crossbill’s dominant competitor for seeds, the red squirrel (Tamiasciurus hudsonicus). Preferential foraging by crossbills on lodgepole pine cones in the South Hills and Albion Mountains, two small mountain ranges in southern Idaho where red squirrels are absent, has led to the evolution of larger, thicker-scaled cones than in nearby ranges where red squirrels are present. This in turn has favored the evolution of larger-billed crossbills that have diverged from other crossbills in the region. However, such diversifying coevolution, resulting from geographic variation in the distribution of strongly interacting species, is vulnerable to species introductions. For example, the introduction of red squirrels caused the precipitous decline and perhaps extinction of the Newfoundland crossbill and perhaps a crossbill endemic to the Cypress Hills, Canada. In general, species introductions act to reduce the geographic variation in species interactions, which may be critical for the diversification of many taxa.
My experiments revealed that two of the call types matched the predicted optima, whereas two others were smaller than predicted (Benkman 1993). That the bill sizes of two of the call types were smaller than predicted did not cause me to reject the hypothesis, in part because I was able to estimate the optimal width of the groove in the crossbill’s palate that is used to secure seeds while they are husked; groove width influences seed handling time, whereas bill depth is related to providing access to seeds in the cones (Fig. 3). In the case of the groove width, each call type matched or closely approximated the predicted optimum (Benkman 1993). Overall, the data were consistent with the hypothesis that each call type was adapted to a single species of conifer. Moreover, I could predict these conifers a priori based on their seed production and seed retention.
Interestingly, I initially hypothesized a fifth key conifer, Sitka spruce (Picea sitchensis), and thus a fifth call type (Benkman 1993). I had gathered foraging data on Sitka spruce cones, and I and my first graduate student, Bill Holimon, searched throughout much of the range of Sitka spruce (rainforests of the Pacific Northwest) for a fifth call type. We did not find it. Over ten years later, however, an astute and diligent field ornithologist, Ken Irwin, living among Sitka spruce in northern California, discovered my hypothesized fifth call type (K. Irwin, unpublished manuscript). He has spent thousands of hours over the last eight years recording and observing this crossbill in the field. This crossbill not only spends nearly all of its time foraging on Sitka spruce, it also has a palate structure that matched what I had predicted over 15 years ago!
Cone Variation, Red Squirrels, and Crossbills
Nine thousand years ago, black spruce (Picea mariana) and presumably crossbills colonized Newfoundland after the glaciers retreated. However, red squirrels and a number of other land mammals did not colonize Newfoundland. In the absence of red squirrels, which are strong competitors for conifer seeds and also strong selective agents on cone structure (Smith 1970), I had argued that crossbills had evolved to exploit cones that had lost their defenses directed at red squirrels (Benkman 1989). Chris Smith had provided compelling evidence that red squirrels coevolved with Rocky Mountain lodgepole pine and that many of its cone traits were related to selection exerted by red squirrels (Smith 1970). Although I suspected that selection exerted on cones by red squirrels had contributed greatly to the evolution of other conifers including black spruce, I still had no evidence that crossbills have an evolutionary effect on conifer cones. I needed to visit the Cypress Hills.
Unfortunately, red squirrels had been introduced to the Cypress Hills in 1950, after Godfrey’s visits (Benkman 1999). Red squirrels were also introduced to Newfoundland in 1963. This latter introduction was to increase the prey base of the over-trapped Newfoundland pine marten (Martes Americana atrata) that numbered in the low hundreds. Although red squirrels spread rapidly across Newfoundland and occur in much higher densities than in comparable forests on the mainland, pine martens have not recovered. Red squirrels have flourished in Newfoundland because in the 9,000 years that black spruce evolved in the absence of red squirrels, the spruce have lost a considerable amount of defense directed at red squirrels. When red squirrels forage on conifer cones, they start at the base and bite off successive scales to reach the underlying seeds that tend to be concentrated at the distal end of the cone. Red squirrels avoid trees whose cones have few seeds and few seeds relative to the mass of cone they need to bite through to reach the seeds. In the absence of red squirrels, the number of seeds per cone increased, and the ratio of cone mass to seed mass in black spruce cones decreased by a third on Newfoundland relative to nearby areas in Quebec where red squirrels are present (Parchman and Benkman 2002). These cone traits appear to be highly heritable, and differences in cone traits among trees appear to represent mainly genetic rather than environmental differences. Those trees that produced less cone mass per seed were presumably at an advantage because they were able to shift their allocation of resources to additional seed production. These black spruce, however, are poorly defended against the introduced red squirrels, which now harvest a vast majority of the cones during autumn soon after the seeds mature (West 1989). This extensive removal of cones by red squirrels may account for the rapid decline of the Newfoundland crossbills beginning about ten years after red squirrels were introduced (Fig. 4b; Benkman 1989; Parchman and Benkman 2002).
The Cypress Hills is orders of magnitude smaller than Newfoundland, and red squirrels were introduced over ten years earlier to the Cypress Hills than to Newfoundland. Thus, if the formerly common Newfoundland crossbill is extinct or at best exceedingly rare (Fig. 4b), I did not hold out much hope for the Cypress Hills crossbill (Fig. 4a). Although I have not conducted extensive surveys in the Cypress Hills, crossbills are uncommon there (Siepielski and Benkman 2005), and we have not detected a distinctive call type. The abundant red squirrels in the Cypress Hills, however, provided an excellent opportunity to measure the selection they exert on lodgepole pine cone morphology.
One fall, while quantifying cone preferences to estimate selection exerted by red squirrels in the Cypress Hills, I came to a vantage point where I could see the similarly isolated and smaller group of mountains, the Sweetgrass Hills, across the border in Montana (Fig. 4a). After finishing our work in the Cypress Hills, we drove to the Sweetgrass Hills. There are only about five square kilometers of lodgepole pine in the Sweetgrass Hills, and there were no red squirrels, and none had been introduced. Cones in both the Cypress and Sweetgrass hills showed evidence of losing defenses directed at red squirrels (58% and 36% decreases, respectively, in the ratios of cone mass to seed mass relative to cones from the Rocky Mountains), having evolved in their absence for probably close to 12,000 years (Benkman 1999). However, the cones in the Sweetgrass Hills, where crossbills were uncommon (Siepielski and Benkman 2005), were smaller, and the scales at the distal end of the cone where crossbills mostly forage (Fig. 1) were thinner than in the Cypress Hills. This variation in scale thickness and the thick distal scales in the Cypress Hills in particular were inconsistent with cone evolution simply in response to selection and relaxation of selection by red squirrels. The obvious explanation was that increased thickness of the distal scales was an evolutionary response to selection exerted by crossbills. Crossbills should avoid cones with thicker distal scales because they would impede crossbills from spreading apart the scales to reach the seeds at the base (Fig. 1b). However, in the absence of a Cypress Hills crossbill to study, I sought additional isolated ranges of lodgepole pine to determine if the differences I had found between the Sweetgrass Hills and the larger-sized Cypress Hills were repeated.
Examining range maps, I located several small isolated ranges west of the Rocky Mountains in southern Idaho where red squirrels were apparently absent and lodgepole pine appeared to occupy about as much area as in the Sweetgrass Hills. I visited the two most isolated ranges, the Albion Mountains and South Hills (Fig. 4a), to collect cones on my way to an ornithology meeting. It turned out the forest maps were inaccurate. The lodgepole pine forests are if anything slightly more extensive than in the Cypress Hills, and the cones were like those in the Cypress Hills (Fig. 4a). Moreover, crossbills were very common, and they even sounded like they might be a different call type. Here was the opportunity to study a crossbill that was potentially coevolving with its food plant. I went to the meeting telling colleagues that I had found a new crossbill.
The next year, I returned to the South Hills to capture crossbills. The crossbills occurred in densities that were about 20 times higher than in lodgepole pine forests in the Rocky Mountains, presumably because their competitor, the red squirrel, was absent (Benkman 1999; Siepielski and Benkman 2005). South Hills Crossbills were larger than other crossbills in western North America, and they had a distinctive call (Fig. 4a). The question remained, were these differences the result of a coevolutionary arms race between crossbills and lodgepole pine in the South Hills? To test this hypothesis, I needed to quantify the forms of selection both exerted and experienced by crossbills. If the selection exerted by crossbills could account for the differences in cone traits between the South Hills and the Rocky Mountains, beyond that resulting from differences in the presence and absence of selection by red squirrels, then this would suggest that crossbills are altering the course of cone evolution. Furthermore, if these differences in cone traits were favoring a larger bill, then these results would support the hypothesis of coevolution.
Our data also indicate that an increase in scale thickness favors larger-billed crossbills, resulting in the evolution of the large-billed crossbills in the South Hills (Benkman et al. 2001, 2003). However, as in my aviary experiments from years before (Benkman 1993), we found that the South Hills crossbill was smaller than that predicted if it was adapted for foraging on the average-sized cone (Benkman et al. 2001, 2003). Although at first I was puzzled by South Hills crossbills having bills smaller than what we initially predicted, in retrospect, this makes sense because crossbills do not forage on average-sized cones. South Hills crossbills preferentially forage on cones that are smaller than average (J. Smith et al., unpublished data). Once we account for this behavior, which is what drives the coevolutionary process in the first place, South Hills crossbills match well what would be predicted based on the cone sizes they mostly forage on (C. W. Benkman, unpublished data).
Let me summarize what we have learned (Fig. 4a). Red squirrels are common throughout most of the range of Rocky Mountain lodgepole pine. They are superior competitors for seeds in the cones and, as a result, crossbills are uncommon in these forests. Selection exerted by red squirrels drives the evolution of cone structure, and crossbills adapt to the average cone. In several isolated mountain ranges east and west of the Rocky Mountains, red squirrels are (were for the Cypress Hills) absent. Here, the pines had lost their defenses directed at red squirrels and, in the absence of red squirrels, crossbills are up to 20 times more abundant than in the Rocky Mountains. Crossbills are now the primary seed predator and exert selection on cone structure favoring the evolution of increased defenses directed at crossbills (i.e., thicker distal scales). This in turn favors the evolution of crossbills with larger bills and over time has favored a continuing escalation in the defenses of pines and the counter-offenses in crossbills, typifying a coevolutionary arms race. Remarkably, we find the pattern of coevolution in the South Hills replicated east of the Rocky Mountains in the Cypress Hills (Fig. 4a). Furthermore, these patterns of cone evolution are strikingly replicated in black spruce in Newfoundland (Fig. 4), and this has all occurred within the last 12,000 years or even less (Benkman et al. 2001; Parchman and Benkman 2002). Now, the South Hills crossbill only rarely interbreeds with other call types that move into the South Hills yearly (Smith and Benkman 2007) and can be considered to represent a distinct species (Loxia sinesciurus or “the crossbill without tree squirrels”; Benkman et al. 2009). Coevolution is clearly a dynamic and powerful force that causes crossbill populations to diverge rapidly and even speciate.
One question remains. How widespread is coevolution in the adaptive radiation of crossbills? We have found similar evidence for evolution in response to selection exerted by crossbills in most of the conifers that crossbills are specialized upon (Benkman et al. in press). This also helps to explain the pattern described earlier for some crossbills matching the optimum bill depth for foraging on their respective key conifers and some having bills smaller than the optimum for foraging on average cones; none have larger bills. As we have discovered repeatedly, crossbills usually forage on smaller than average-sized cones of their respective key conifers (Benkman et al. 2003; Parchman and Benkman 2008; Benkman and Parchman 2009; Mezquida and Benkman in press), presumably because this allows them to have higher feeding intake rates (Benkman 1999). Those crossbills, for which we have evidence of their either exerting selection on their key conifers, or evolution of increased crossbill defenses in their key conifers, are the crossbills having smaller than “optimal” bills (the Douglas-fir [call type 4], ponderosa pine [call type 2], and South Hills [call type 9] crossbills; Benkman et al. in press). In contrast, those crossbills for which we have no evidence of their exerting selection on cone structure match the predicted optima (lodgepole pine [call type 5] and western hemlock [call type 3] crossbills—although the hemlock crossbill appears not to preferentially forage on smaller cones, it apparently exerts selection on seed coat structure; Benkman et al. in press).
In conclusion, coevolution is an important process in the diversification of crossbills, and examining how this process manifests itself has helped us unravel the patterns of diversification in crossbills. In addition, our studies reveal that variation in the distribution of co-occurring species has caused geographic variation in coevolution (geographic mosaic of coevolution; see Thompson in this volume). Other investigators have found that geographic variation in the occurrence and outcome of coevolution arises because of variation in the distribution of co-occurring species, including competitors (Craig et al. 2007), alternative hosts (Zangerl and Berenbaum 2003), and co-pollinators (Thompson and Fernandez 2006; see Thompson in this volume). In our studies, discontinuities in the distribution of other species or variation in the species composition of communities (i.e., community context) arise because of biogeographical factors differentially limiting dispersal (large treeless expanses preventing red squirrels but not birds from colonizing forests: e.g., Benkman et al. 2001; Siepielski and Benkman 2007). In other studies, geographic variation arises because the distributions of some but not all interacting species span two adjacent biomes (e.g., prairie and forest: Craig et al. 2007). If variation in the species composition of communities (i.e., community context) is what often generates geographic variation, then we need to minimize the introduction of species, even species from nearby areas. Introductions of species, especially strongly interacting species like red squirrels, not only cause extinctions but also act to homogenize interactions across the landscape (Benkman et al. 2008). Without this geographic variation, speciation and diversification will be impeded (Mayr 1963; Coyne and Orr 2004), and future opportunities for diversification will be lost.
The National Geographic Society, NSERC, and especially the National Science Foundation (most recently DEB-0344503 and DEB-0455705) have funded most of my research on crossbills. I thank the editors, R. Medel and J. N. Thompson, for inviting me to write this paper, and J. Hart, T. Parchman, A. Siepielski, L. Throop, an anonymous reviewer, and the editors for commenting on the manuscript.
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