Nearly 15 years ago we found evidence for coevolution between crossbills (Loxia) and lodgepole pine (Pinus contorta latifolia). Because it was so striking, we began examining other crossbill-conifer systems to (1) see how common coevolution is in the adaptive radition of crossbills and (2) determine the conditions that favor and disfavor coevolutionary arms races. This has taken us across North America, to Hispaniola and the Mediterranean, and most recently to Vietnam and the Philippines. We have found evidence for coevolution in most crossbill populations that we've studied and are beginning to understand the various factors that influence species interaction strength, including the presence and absence of preemptive competitors (tree squirrels), resource stability, and habitat area and structure, and how this alters the form and strength of phenotypic selection and coevolution. Here are our publications related to this research (many can be downloaded from my "publications" page). See CourseSource for a coevolution lesson plan based on the coevolutionary interactions between crossbills, squirrels and lodgepole pine.
Benkman, C. W., and E. T. Mezquida. 2015. Phenotypic selection exerted by a seed predator is replicated in space, time, and among prey species. American Naturalist 186:682-691.
Mezquida, E. T., and C. W. Benkman. 2014. Causes of variation in biotic interaction strength and phenotypic selection along an altitudinal gradient. Evolution 68:1710–21.
Benkman, C. W. 2013. Biotic interaction strength and the intensity of selection. Ecology Letters 16:1054-1560.
Benkman, C. W., and T. L. Parchman. 2013. When directional selection reduces geographic variation in traits mediating species interactions. Ecology and Evolution 3:961-970.
Benkman, C. W., J. W. Smith, M. Maier, L. Hansen, and M. V. Talluto. 2013. Consistency and variation in phenotypic selection exerted by a community of seed predators. Evolution 67:157-169.
Parchman, T. L., C. W. Benkman, B. Jenkins, and C. A. Buerkle. 2011. Low levels of population genetic structure in lodgepole pine across a geographic mosaic of coevolution. American Journal of Botany 98:669-679.
Benkman C. W., T. L. Parchman, and E. T. Mezquida. 2010. Patterns of coevolution in the adaptive radiation of crossbills. Annals of the New York Academy of Sciences 1206:1-16.
Mezquida, E. T., and C. W. Benkman. 2010. Habitat area and structure affect the impact of seed predators and the potential for coevolutionary arms races. Ecology 91:802-814.
Benkman, C. W. 2010. Diversifying coevolution between crossbills and conifers. Evolution: Education and Outreach 3:47-53.
Benkman, C. W., and T. L. Parchman. 2009. Coevolution between crossbills and black pine: the importance of competitors, forest area, and resource stability. Journal of Evolutionary Biology 22:942-953.
Parchman, T. L., and C. W. Benkman. 2008. The geographic selection mosaic for ponderosa pine and crossbills: a tale of two squirrels. Evolution 62:348-360.
Parchman, T. L., C. W. Benkman, and E. T. Mezquida. 2007. Coevolution between Hispaniolan Crossbills and pine: Does more time allow for greater phenotypic escalation at lower latitude? Evolution 61:2142-2153.
Edelaar, P., and C. W. Benkman. 2006. Replicated population divergence caused by localised coevolution? A test of three hypotheses in the red crossbill-lodgepole pine system. Journal of Evolutionary Biology 19:1651-1659.
Siepielski, A. M., and C. W. Benkman. 2005. A role for habitat area in the geographic mosaic of coevolution between Red Crossbills and lodgepole pine. Journal of Evolutionary Biology 18:1042-1049.
Mezquida, E. T., and C. W. Benkman. 2005. The geographic selection mosaic for squirrels, crossbills and Aleppo pine. Journal of Evolutionary Biology 18:348-357.
Siepielski, A. M., and C. W. Benkman. 2004. Interactions among moths, crossbills, squirrels and lodgepole pine in a geographic selection mosaic. Evolution 58:95-101.
Benkman, C. W., T. L. Parchman, A. Favis, and A. M. Siepielski. 2003. Reciprocal selection causes a coevolutionary arms race between crossbills and lodgepole pine. American Naturalist 162: 182-194.
Parchman, T. L., and C. W. Benkman. 2002. Diversifying coevolution between crossbills and black spruce on Newfoundland. Evolution 56:1663-1672.
Benkman, C. W., W. C. Holimon, and J. W. Smith. 2001. The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine. Evolution 55:282-294.
Benkman, C. W. 1999. The selection mosaic and diversifying coevolution between crossbills and lodgepole pine. American Naturalist 154:S75-S91.
We have also examined how ecological adaptation as a result of divergent selection has led to reproductive isolation. The South Hills Crossbill has diverged not only in bill size (they are larger than other crossbills in the region) but also in calls and song. We have found extremely high levels of reproductive isolation between the South Hills Crossbill and the two other Red Crossbill call types that breed in the South Hills. Much of the premating reproductive isolation is the result of South Hills Crossbills depressing seed availability so that other crossbills with smaller (less efficient) bills are unable to persist and breed. In addition, South Hills Crossbills preferentially pair with other South Hills Crossbills. Because the South Hills Crossbills are so divergent from other crossbills and levels of reproductive isolation are so high, we recently argued that they should be recognized as a new species. We are now using high-throughput sequencing to characterize genetic variation among different taxa of crossbills, and we are further characterizing the levels of premating reproductive isolation among other call types. Below are some publications related to ecological speciation and mate choice in South Hills Crossbills (some can be downloaded from my "publications" page).
Smith, J. W., S. M. Sjoberg, M. C. Mueller, and C. W. Benkman. 2012. Assortative flocking in crossbills and implications for ecological speciation. Proceedings of the Royal Society of London Series B 279:4223-4229.
Snowberg, L. K., and C. W. Benkman 2009. Mate choice based on a key ecological performance trait. Journal of Evolutionary Biology 22:762-769.
Benkman, C. W., J. W. Smith, P. C. Keenan, T. L. Parchman, and L. Santisteban. 2009. A new species of Red Crossbill (Fringillidae: Loxia) from Idaho. Condor 111: 169-176.
Keenan, P. C., and C. W. Benkman. 2008. Call imitation and call modification in Red Crossbills. Condor 110:93-101.
Snowberg, L. K., and C. W. Benkman. 2007. The role of marker traits in the assortative mating within Red Crossbills, Loxia curvirostra complex. Journal of Evolutionary Biology 20:1924-1932.
Smith, J. W., and C. W. Benkman. 2007. A coevolutionary arms race causes ecological speciation in crossbills. American Naturalist 169:455-465.
Smith, J. W., C. W. Benkman, and K. Coffey. 1999. The use and mis-use of public information by foraging red crossbills. Behavioral Ecology 10:54-62.
The South Hills crossbill has declined by over 80 percent between 2003 and 2012. This decline is most likely the result of increasing numbers of hot summer days (>32 C), which are causing serotinous lodgepole pine cones to open and prematurely shed their seeds. We continue to study the decline and its causes using mark-recapture methods. Below is the one paper we have published on this; more recent analyses (through 2015) support the conclusions in this paper and to our relief the population is rebounding due to almost no hot summer days in the last six years.
Santisteban, L., C. W. Benkman, T. Fetz, and J. W. Smith. 2012. Survival and population size of a resident bird species are declining as temperature increases. Journal of Animal Ecology 81:352–363.
Previous research on serotiny, a key life history trait for woody plants occurring in fire-prone habitats, has focused on fire where increasing fire frequency favors higher frequencies of serotiny. In contrast, we find that the dominant seed predator, the red squirrel, which harvests proportionately more serotinous than nonserotinous lodgepole pine cones, strongly selects against serotiny and can overwhelm selection from fire. Thus, the frequency of serotiny in lodgepole pine varies across the landscape depending on both fire frequency and the density of red squirrels. Based on recent unpublished work, the latter seems to be influenced by features of the soil and in turn forest structure and likely fungi abundance. This is of considerable interest as the frequency of serotiny influences the number of seeds in the canopy seed bank and the number of seedlings following a fire with community and ecosystem effects. See A Small Mammal With Outsized Impact, a post of our blog on this topic.
Talluto, M. V., and C. W. Benkman. 2014. Conflicting selection from fire and seed predation drives fine-scaled phenotypic variation in a widespread North American conifer. Proceedings of the National Academy of Sciences USA 111:9543-9548.
Talluto, M. V., and C. W. Benkman. 2013. Landscape-scale eco-evolutionary dynamics: selection by seed predators and fire determine a major reproductive strategy. Ecology 94:1307-1316.
Parchman, T. L., Z. Gompert, J. Mudge, F. D. Schilkey, C. W. Benkman, and C. A. Buerkle. 2012. Genome-wide association genetics of an adaptive trait in lodgepole pine. Molecular Ecology 21:2991-3005.
Benkman, C. W., A. M. Siepielski, and J. W. Smith. 2012. Consequences of trait evolution in a multi-species system. Pages 278-292 in Interaction Richness and Complexity: Ecological and Evolutionary Aspects of Trait-Mediated Indirect Interactions. T. Ohgushi, O. Schmitz, and R. Holt, eds. Cambridge University Press.
Benkman, C. W., and A. M. Siepielski. 2004. A keystone selective agent? Pine squirrels and the frequency of serotiny in lodgepole pine. Ecology 85:2082-2087.
Our interest is in understanding how the presence and absence of a superior preemptive competitor (pine squirrels Tamiasciurus) has affected the evolution of seed dispersal by Clark's Nutcrackers (Nucifraga columbiana) in limber pine (Pinus flexilis) and whitebark pine (P. albicaulis) and how this affects the ecology of the pines. Below are our publications related to this research.
Benkman, C. W., and A. M. Siepielski. 2011. Sources and sinks in the
evolution and persistence of mutualisms. Pages 82-98 in Sources, Sinks, and Sustainability. J. Liu, V. Hull, A. Morzillo, and J. Wiens, eds. Cambridge University Press.
Siepielski, A. M., and C. W. Benkman. 2010. Conflicting selection from an antagonist and a mutualist enhances phenotypic variation in a plant. Evolution 64:1120-1128.
Garcia, R., A. M. Siepielski, and C. W. Benkman. 2009. Cone and seed trait variation in whitebark pine Pinus albicaulis (Pinaceae) and the potential for phenotypic selection. American Journal of Botany 96:1050-1054.
Siepielski, A. M., and C. W. Benkman. 2008. A seed predator drives the evolution of a seed dispersal mutualism. Proceedings of the Royal Society of London Series B. 275:1917-1925.
Siepielski, A. M., and C. W. Benkman. 2008. Seed predation and selection exerted by a seed predator influence subalpine tree densities. Ecology 89:2960-2966.
Siepielski, A. M., and C. W. Benkman. 2007. Extreme environmental variation sharpens selection that drives the evolution of a mutualism. Proceedings of the Royal Society of London Series B 274:1799-1805.
Siepielski, A. M., and C. W. Benkman. 2007. Selection by a pre-dispersal seed predator constrains the evolution of avian seed dispersal in pines. Functional Ecology 21:611-618.
Siepielski, A. M., and C. W. Benkman. 2007. Convergent patterns in the selection mosaic for two North American bird-dispersed pines. Ecological Monographs 77:203-220.
Benkman, C. W. 1995. The impact of tree squirrels (Tamiasciurus) on limber pine seed dispersal adaptations. Evolution 49:585-592.
Benkman, C. W. 1995. Wind dispersal capacity of pine seeds, with comments on the evolution of different seed dispersal modes in pines. Oikos 73: 221-224.
Benkman, C. W., R. P. Balda, and C. C. Smith. 1984. Adaptations for seed dispersal and the compromises due to seed predation in limber pine. Ecology 65:632-642.
Two short articles that Adam Siepielski wrote concerning his research on nutcrackers, pine squirrels, and white pines can be downloaded below:
See the following website for general information on High Elevation White Pines and their conservation