The genomic divergence of crossbills in Europe

Blog post by Dr Ron Summers, Principal Conservation Scientist, RSPB Centre for Conservation Science.

The stability of cone crops and geographic isolation are linked to the genomic divergence of crossbills in Europe

Crossbills are finches with a peculiar bill, adapted to prise open the scales of closed and opening conifer cones to access the seeds. They occur throughout most of the conifer woodlands of the northern hemisphere.

Those in Europe are split into three species according to morphological differences: parrot crossbill Loxia pytyopsittacus, Scottish crossbill L. scotica and common crossbill L. curvirostra.

Photograph 1. A male common crossbill of the Balearic subspecies, L. c. balearica. Photo by Ron Summers.

Species differences

These species differ in average bill size: parrot crossbills have the largest bill; common crossbills the smallest; and Scottish crossbills are intermediate between the other two. These differences reflect differences in the main conifers they exploit for food.

Both parrot and Scottish crossbills are linked to Scots pine Pinus sylvestris, though the Scottish crossbill also has a strong association with the introduced lodgepole pine Pinus contorta. In northern Europe, common crossbills are associated with the Norway spruce Picea abies.

Both Scots pine and Norway spruce vary in their cone production between years, such that in years of poor or no cone production, there are irruptions of common and parrot crossbills to other parts of their ranges.

In the Mediterranean

The common crossbill has been split into subspecies, particularly within the Mediterranean region: L.c. balearica (from the Balearic Islands) (Photograph 1), L.c. poliogyna (Morocco), L.c. guillemardi (Cyprus), L.c. corsicana (Corsica) and L.c. hispana (southeast Spain). The nominate subspecies (curvirostra) occurs across northern Europe, and often irrupts into Britain, where they also breed.

Photograph 2. Aleppo pine woodland in Majorca. Photo by Ron Summers.

The Mediterranean subspecies feed mainly on the seeds of the Aleppo pine (Pinus halepensis) (Photographs 2 and 3). This pine tends to produce a similar size of cone crop each year, and it also retains its cones, rather than shed them after seeding (eg the Scots pine drops its cones after shedding the seeds).

The retention of cones (serotiny) is an adaptation by pines prone to fire. Cones may be opened by the heat of fire, and resulting seeds fall onto burnt ground where they have an excellent chance to establish.

Early attempts to determine if there are genetic differences among the different crossbill taxa failed, probably because only a small part of the genome was investigated (Questiau et al. 1999). For example, when Piertney et al. (2001) compared five microsatellite loci and sequenced the mitochondrial control region from parrot, Scottish and common crossbills, no evidence of genetic structuring was found.

Photograph 3. Aleppo pines cones of two cohorts in Majorca, where the Balearic crossbill occurs. The older cone has opened in the absence of fire. Photo by Ron Summers.

The study and results

The ability to make genetic comparisons has moved on, such that it now possible to examine a greater amount of the genome. I took part in an international study that examined four subspecies of common crossbill (balearica, poliogyna, hispana and curvirostra) and parrot crossbills.

The curvirostra material came from the Pyrenees and Scotland. I also split my sample from Scotland into call-types, now that differences in average size have been found according to call-type (Edelaar et al. 2008, RS unpublished data). Material from L. scotica could not be amplified for genetic analysis.

There were clear patterns of divergence for the subspecies associated with the Aleppo pine (balearica, poliogyna and hispana). Thus, it seems that both geographical isolation and a stable food resource may have contributed to the divergence of balearica and poliogyna.

The hispana crossbills on mainland Spain are less isolated than the other two subspecies, so that only the stable cone production of Aleppo pine was linked to their residency and genetic divergence.

By contrast, there was no evidence of divergence between common crossbills from the Pyrenees and Scotland, and no divergence according to the two call-types, 1A and 4E. These crossbill groups are associated with less stable cone cropping and are prone to large scale movements.

Interestingly, there was only a slight differentiation between common and parrot crossbills. This suggests that despite the large morphological difference between common and parrot crossbills (there is no overlap in bill depths), there must be some gene flow (cross-mating) to account for the lack of greater divergence.

Full paper:

Parchman, T.L., Edelaar, P., Uckele, K., Mezquida, E.T., Alonso, D., Jahner, J.P., Summers, R.W. & Benkman, C.W. 2018. Resource stability and geographical isolation are associated with genomic divergence in western Palaearctic crossbills. Journal of Evolutionary Biology doi: 10.1111/jeb.13367.

References:

Edelaar, P., van Eerde, K. & Terpstar, K. 2008. Is the nominate subspecies of the Common Crossbill Loxia c. curvirostra polytypic? II. Differentiation among vocal types in functional traits. Journal of Avian Biology 39, 108-115.

Piertney, S.B., Summers, R.W & Marquiss, M. 2001 Microsatellite and mitochondrial DNA homogeneity among phenotypically diverse crossbill taxa in the UK. Proceedings of the Royal Society, London B, 268, 1511-1517.

Questiau, S., Gielly, L., Clouet, M. and Taberlet, P. 1999. Phylogeographical evidence of gene flow among Common Crossbills (Loxia curvirostra, Aves, Fringillidae) populations at the continental level. Heredity 83, 196-205.