Response to Lundmark: Polyploidization, hybridization and geographical parthenogenesis

Abstract

In his letter to TREE [1xSee all References[1], Lundmark emphasizes that polyploidy per se might have an important influence on the ecological success and geographical patterns of parthenogenetic organisms, independent of the effects of hybridization. In support of this, he cites several cases of apparent autopolyploidy in sexual and asexual organisms that exhibit similar geographical tendencies to those described under the umbrella of geographical parthenogenesis. Although this might apply to some situations, I see two difficulties in attributing polyploidy to the geographical patterns of parthenogenesis. One lies in excluding some level of hybridization within cases of ‘autopolyploid’ parthenogenesis, and the other in explaining mechanistically how hybridization and polyploidy could independently lead to similar geographical patterns.The first problem relates to the exclusion of hybridization as a hypothesis. In its broadest sense, hybridization can be considered as the interbreeding of two populations that are distinct on the basis of one or more heritable characters [2xNatural Hybridization and Evolution. Arnold, M.J. See all References, 3xChromosome Evolution in Higher Plants. Stebbins, G.L. See all References]. Given that the term ‘autopolyploid’ is typically used to refer to cases of polyploidy arising within species, this leads to the possibility of a hybrid ‘autopolyploid’ if polyploidy arises from a cross between ecologically differentiated races [2xNatural Hybridization and Evolution. Arnold, M.J. See all References[2]. Indeed, apparent cases of ‘autopolyploid’ parthenogenesis can exhibit higher genetic diversity within and between individuals than expected based on local sexual populations, suggesting secondary contact and hybridization (e.g. [4xPhylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: patterns and explanations. Pongratz, N. et al. BMC Evol. Biol. 2003; 3Crossref | PubMed | Scopus (48)See all References[4]). Thus, the key issue is whether we can find geographical parthenogenesis in polyploids that have clearly arisen from genome duplications within a particular individual, population or race, rather than from crosses between distinct populations or races. Only in the former case would there be a strong argument that an increase in chromosome number itself is providing an advantage. Otherwise, the hybrid state could be driving the advantage, and the polyploid state could merely represent the fact that a parthenogen cannot normally ‘hybridize’ with a sexual lineage without gaining an additional genome. The same arguments also apply to cases of sexual autopolyploids exhibiting similar patterns to geographical parthenogenesis. The significance of polyploidy in sexual cases, however, would be its capacity to buffer and preserve advantageous gene combinations acquired via hybridization [5xPolyploidy, hybridization, and the invasion of new habitats. Stebbins, G.L. Ann. Mo. Bot. Gard. 1985; 72: 824–832CrossrefSee all References[5]. Unfortunately, hybridization, even between species, is often difficult to detect (e.g. [6xPhylogenetic evidence for hybrid origins of asexual lineages in an aphid species. Delmotte, F. et al. Evolution. 2003; 57: 1291–1303PubMedSee all References[6]).If there were cases of geographical parthenogenesis in truly non-hybrid autopolyploids, this would suggest that hybridization and polyploidy can both result independently in similar ecological and geographical patterns. This leads to the second difficulty: what effects do hybridization and polyploidy have in common that could lead to these similar patterns? I emphasized that an advantage provided by hybridization in open, novel environments could arise either through the generation of phenotypic novelty, or through the enhancement of genetic diversity [7xHybridization, glaciation and geographical parthenogenesis. Kearney, M. Trends Ecol. Evol. 2005; 20: 495–502Abstract | Full Text | Full Text PDF | PubMed | Scopus (148)See all References[7]. There is some evidence that polyploidy can also lead to phenotypic novelty by triggering changes in gene expression, although hybridization is also often involved in these cases [8xGenes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Adams, K.L. et al. Proc. Natl. Acad. Sci. U. S. A. 2003; 100: 4649–4654Crossref | PubMed | Scopus (498)See all References[8]. Another possibility is that polyploidy and hybridization are both acting principally to mask deleterious alleles, via polysomic inheritance or dominance complementation, respectively. If this is true, we would expect to see polyploidy and hybridization associated with the invasion of open environments in species that are prone to significant genetic loads or inbreeding levels, perhaps resulting from patchy and fragmented distributions, as often occurs for instance in Daphnia [9xBiogeography of parthenogenetic animals. Cuellar, O. Biogeographica. 1994; 70: 1–13See all References[9]. From this point of view, it is interesting that many parthenogenetic organisms exhibiting geographical parthenogenesis have low vagility, with many insect examples being wingless [10xA new hypothesis to explain geographic parthenogenesis. Haag, C. and Ebert, D. Ann. Zool. Fenn. 2004; 41: 539–544See all References[10], including the grasshopper Warramaba virgo, moths of the genus Dahlica (formerly Solenobia), and weevils of the genus Otiorhynchus.