How do we address the disconnect between genetic and morphological diversity in germplasm collections?

Th e world’s food production systems must keep up with an everincreasing demand in spite of the challenges caused by climate change and environmental degradation. To meet this challenge, plant breeders must have access to genetic diversity for crop improvement. However, genetic homogeneity in the handful of major crops that feed the world limits options for breeding progress ( Swaminathan, 2009 ). Wild and landrace relatives of crop plants provide much needed diversity and are maintained in gene banks worldwide ( McCouch, 2013 ). Th is germplasm resource is underused by breeders, mainly because genotypic and phenotypic data are limited. However, using rapidly developing genomics resources, breeders are unlocking the genetic potential in gene banks and making remarkable advances ( Tanksley and McCouch, 1997 ). Morphological traits and neutral genetic markers are commonly used to characterize germplasm collections, with the goal of improving the value of these collections to breeders ( Brown, 1989 ). Morphological and neutral marker data provide the foundation for the assembly of a core collection, defi ned as a subset of a germplasm collection intended to represent the entire collection. Th e concept of a core collection assumes that the core has some utility for plant improvement. Th at is, the core collection is maximally diverse and is useful for breeding. Evaluating the core collection for key traits should also have some level of predictability for the rest of the collection based on the relatedness of core accessions to other accessions in the collection. It has been recognized for many years that morphological traits do not always provide a good measure of genetic values and may not accurately reveal the genetic variation in a germplasm collection ( Tanksley and McCouch, 1997 ). Consequently, neutral molecular markers have become popular because they are thought to more accurately refl ect genetic relationships in germplasm collections ( Ebana et al., 2008 ). But genetic relatedness measures based on neutral markers may not predict similarity in trait values or parental performance. Th e patterns of allelic variation in a species may be very diff erent for neutral markers compared with genes under selection. Based on a meta-analysis, McKay and Latta (2002) argued that allele frequencies at neutral and selected loci are not correlated because evolutionary forces act diff erently on them. A meta-analysis by Reed and Frankham (2001) showed only weak correlation between neutral molecular markers and quantitative measures of variation. Reeves, Panella, and Richards (2012) found that genetic variation at loci of agronomic interest in core collections assembled using neutral diversity may be lower than in collections assembled at random. In addition, neutral genetic markers identifi ed in single populations or breeding lines may have signifi cant ascertainment bias, which makes them unrepresentative of the full range of functional genetic diversity in the species ( Moragues et al., 2010 ). Our breeding research in potato has revealed a remarkably unexpected result that has led us to question the value of morphological diversity as a proxy for overall genetic diversity. We assessed an F 2 population created by self-pollinating an F 1 clone from a cross between two diploid (2 n = 2 × = 24) potato clones: DM, a completely homozygous clone derived from somatically doubling an androgenic monoploid of a cultivated potato, and M6, a highly inbred clone derived from seven generations of self-pollination of the wild diploid potato relative Solanum chacoense. We evaluated the F 2 population for a variety of morphological features including tuber size, shape, and eye depth; skin and flesh color; and dry matter content. Phenotypic segregation in this F 2 population is astounding ( Fig. 1 ). Th e tuber shape and color variability derived from self-pollinating a single diploid F 1 plant approaches that of the landrace collections maintained in potato genebanks ( Spooner and Hetterscheid, 2005 ) ( Fig. 1 ). 1 Manuscript received 6 May 2015; revision accepted 11 June 2015. 2 USDA-Agricultural Research Service, Vegetable Crops Research Unit, University of Wisconsin, 1575 Linden Drive, Madison, Wisconsin; and 3 Department of Horticulture, University of Wisconsin-Madison, 1575 Linden Drive, Madison, Wisconsin 53706-1590 USA 4 Author for correspondence: (e-mail: shelley.jansky@ars.usda.gov) doi:10.3732/ajb.1500203 O N T H E N AT U R E O F T H I N G S : E S S AYS