olution Vol.21 No.1 January 2006

Update TRENDS in Ecology and Ev10

Letters Response

Response to Lundmark: Polyploidization, hybridizationand geographical parthenogenesis

Michael Kearney

Centre for Environmental Stress and Adaptation Research, The University of Melbourne, Parkville, VIC 3010, Australia

In his letter to TREE [1], Lundmark emphasizes thatpolyploidy per se might have an important influence onthe ecological success and geographical patterns ofparthenogenetic organisms, independent of the effects ofhybridization. In support of this, he cites several casesof apparent autopolyploidy in sexual and asexualorganisms that exhibit similar geographical tendenciesto those described under the umbrella of geographicalparthenogenesis. Although this might apply to somesituations, I see two difficulties in attributing polyploidyto the geographical patterns of parthenogenesis. One liesin excluding some level of hybridization within cases of‘autopolyploid’ parthenogenesis, and the other in explain-ing mechanistically how hybridization and polyploidycould independently lead to similar geographical patterns.

The first problem relates to the exclusion of hybridizationas a hypothesis. In its broadest sense, hybridization can beconsidered as the interbreeding of two populations that aredistinctonthe basis ofone ormoreheritable characters [2,3].Given that the term ‘autopolyploid’ is typically used to referto cases of polyploidy arising within species, this leads to thepossibility of a hybrid ‘autopolyploid’ if polyploidy arisesfrom a cross between ecologically differentiated races [2].Indeed, apparent cases of ‘autopolyploid’ parthenogenesiscan exhibit higher genetic diversity within and betweenindividuals than expected based on local sexual populations,suggesting secondary contact and hybridization (e.g. [4]).Thus, the key issue is whether we can find geographicalparthenogenesis in polyploids that have clearly arisen fromgenome duplications within a particular individual, popu-lation or race, rather than from crosses between distinctpopulations or races. Only in the former case would there bea strong argument that an increase in chromosome numberitself is providing an advantage. Otherwise, the hybrid statecould bedriving the advantage, and the polyploid state couldmerely represent the fact that a parthenogen cannotnormally ‘hybridize’ with a sexual lineage without gainingan additional genome. The same arguments also apply tocases of sexual autopolyploids exhibiting similar patterns togeographical parthenogenesis. The significance of poly-ploidy in sexual cases, however, would be its capacity tobuffer and preserve advantageous gene combinationsacquired via hybridization [5]. Unfortunately, hybridiza-tion, even between species, is often difficult to detect (e.g.[6]).

If there were cases of geographical parthenogenesis intruly non-hybrid autopolyploids, this would suggest

Corresponding author: Kearney, M. (mrke@unimelb.edu.au).Available online 8 November 2005

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that hybridization and polyploidy can both resultindependently in similar ecological and geographicalpatterns. This leads to the second difficulty: what effectsdo hybridization and polyploidy have in common that couldlead to these similar patterns? I emphasized that anadvantage provided by hybridization in open, novelenvironments could arise either through the generationof phenotypic novelty, or through the enhancement ofgenetic diversity [7]. There is some evidence that poly-ploidy can also lead to phenotypic novelty by triggeringchanges in gene expression, although hybridization is alsooften involved in these cases [8]. Another possibility is thatpolyploidy and hybridization are both acting principally tomask deleterious alleles, via polysomic inheritance ordominance complementation, respectively. If this is true,we would expect to see polyploidy and hybridizationassociated with the invasion of open environments inspecies that are prone to significant genetic loads orinbreeding levels, perhaps resulting from patchy andfragmented distributions, as often occurs for instance inDaphnia [9]. From this point of view, it is interesting thatmany parthenogenetic organisms exhibiting geographicalparthenogenesis have low vagility, with many insectexamples being wingless [10], including the grasshopperWarramaba virgo, moths of the genus Dahlica (formerlySolenobia), and weevils of the genus Otiorhynchus.

References

1 Lundmark, M. (2005) Polyploidization, hybridization and geographi-cal parthenogenesis. Trends Ecol. Evol. 21, doi: 10.1016/j.tree.2005.10.007

2 Arnold, M.J. (1997) Natural Hybridization and Evolution, OxfordUniversity Press

3 Stebbins, G.L. (1971) Chromosome Evolution in Higher Plants,Edward Arnold

4 Pongratz, N. et al. (2003) Phylogeography of competing sexual andparthenogenetic forms of a freshwater flatworm: patterns andexplanations. BMC Evol. Biol. 3. doi: 10.1186/1471-2148-3-23

5 Stebbins, G.L. (1985) Polyploidy, hybridization, and the invasion ofnew habitats. Ann. Mo. Bot. Gard. 72, 824–832

6 Delmotte, F. et al. (2003) Phylogenetic evidence for hybrid origins ofasexual lineages in an aphid species. Evolution 57, 1291–1303

7 Kearney, M. (2005) Hybridization, glaciation and geographicalparthenogenesis. Trends Ecol. Evol. 20, 495–502

8 Adams, K.L. et al. (2003) Genes duplicated by polyploidy showunequal contributions to the transcriptome and organ-specificreciprocal silencing. Proc. Natl. Acad. Sci. U. S. A. 100, 4649–4654

9 Cuellar, O. (1994) Biogeography of parthenogenetic animals. Biogeo-graphica 70, 1–13

10 Haag, C. and Ebert, D. (2004) A new hypothesis to explain geographicparthenogenesis. Ann. Zool. Fenn. 41, 539–544

0169-5347/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.tree.2005.10.013