Coevolution Between Hispaniolan Crossbills and Pine: Does More Time Allow for Greater Phenotypic Escalation at Lower Latitude?

Abstract

Crossbills (Aves: Loxia) and several conifers have coevolved in predator-prey arms races over the last 10,000 years. However, the extent to which coevolutionary arms races have contributed to the adaptive radiation of crossbills or to any other adaptive radiation is largely unknown. Here we extend our previous studies of geographically structured coevolution by considering a crossbill-conifer interaction that has persisted for a much longer time period and involves a conifer with more variable annual seed production. We examined geographic variation in the cone and seed traits of two sister species of pines, Pinus occidentalis and P. cubensis, on the islands of Hispaniola and Cuba, respectively. We also compared the Hispaniolan crossbill (Loxia megaplaga) to its sister taxa the North American white-winged crossbill (Loxia leucoptera leucoptera). The Hispaniolan crossbill is endemic to Hispaniola whereas Cuba lacks crossbills. In addition and in contrast to previous studies, the variation in selection experienced by these pines due to crossbills is not confounded by the occurrence of selection by tree squirrels (Tamiasciurus and Sciurus). As predicted if P. occidentalis has evolved defenses in response to selection exerted by crossbills, cones of P. occidentalis have scales that are 53% thicker than those of P. cubensis. Cones of P. occidentalis, but not P. cubensis, also have well-developed spines, a known defense against vertebrate seed predators. Consistent with patterns of divergence seen in crossbills coevolving locally with other conifers, the Hispaniolan crossbill has evolved a bill that is 25% deeper than the white-winged crossbill. Together with phylogenetic analyses, our results suggest that predator-prey coevolution between Hispaniolan crossbills and P. occidentalis over approximately 600,000 years has caused substantial morphological evolution in both the crossbill and pine. This also indicates that cone crop fluctuations do not prevent crossbills and conifers from coevolving. Furthermore, because the traits at the phenotypic interface of the interaction apparently remain the same over at least several hundred thousand years, divergence as a result of coevolution is greater at lower latitude where crossbill-conifer interactions have been less interrupted by Pleistocene events.

Origin, paleoecology, and extirpation of bluebirds and crossbills in the Bahamas across the last glacial–interglacial transition

“…25) have followed Bond (26) in considering L. megaplaga to be a subspecies of the white-winged crossbill (Loxia leucoptera), which otherwise inhabits boreal or cool temperate parts of North America (L. l. leucoptera) and Eurasia (the larger L. l. bifasciata). We follow Wetmore and Swales (27) in regarding L. megaplaga as endemic to Hispaniola, a judgment supported by molecular data (28,29) and osteological data presented in this paper.…”

“…bahamensis, the only pine in the Bahamas, has cones that average longer but not wider or heavier, cone scales that are thinner, and seeds that are much lighter (SI Appendix, Table S5). Scale thickness of the Bahamian pine falls between the values for Pinus cubensis and P. occidentalis measured by Parchman et al (29), who argued that the thick scales of P. occidentalis (thicker than in P. cubensis) had evolved as a defense to seed predation by L. megaplaga.…”

“…In size, the Bahamian crossbill fossils also resemble both modern and fossil L. megaplaga specimens from Hispaniola (SI Appendix, Table S4). This species is much larger than in any modern specimens of L. leucoptera, its continental sister species based on molecular data (28,29) and plumage (white wing bars). James (34) distinguished L. leucoptera from Loxia curvirostra by the number of fused thoracic vertebrae in the notarium (three in the former, two in the latter).…”

“…29, table 2 therein), P. caribaea var. bahamensis, the only pine in the Bahamas, has cones that average longer but not wider or heavier, cone scales that are thinner, and seeds that are much lighter (SI Appendix, Table S5).…”

“…Such shifts in food habits might help to explain the low SDM climatic suitability scores of crossbills on the North American mainland versus those of the extirpated population in the Bahamas. Parchman et al (29) suggested that coevolution with L. megaplaga led to the thicker cone scales in P. occidentalis. In the ice-age Bahamas, L. megaplaga presumably fed on the seeds of P. caribaea var.…”