Species History Masks the Effects of Human-Induced Range Loss – Unexpected Genetic Diversity in the Endangered Giant Mayfly Palingenia longicauda

Freshwater biodiversity has declined dramatically in Europe in recent decades. Because of massive habitat pollution and morphological degradation of water bodies, many once widespread species persist in small fractions of their original range. These range contractions are generally believed to be accompanied by loss of intraspecific genetic diversity, due to the reduction of effective population sizes and the extinction of regional genetic lineages. We aimed to assess the loss of genetic diversity and its significance for future potential reintroduction of the long-tailed mayfly Palingenia longicauda (Olivier), which experienced approximately 98% range loss during the past century. Analysis of 936 bp of mitochondrial DNA of 245 extant specimens across the current range revealed a surprisingly large number of haplotypes (87), and a high level of haplotype diversity (). In contrast, historic specimens (6) from the lost range (Rhine catchment) were not differentiated from the extant Rába population (, ), despite considerable geographic distance separating the two rivers. These observations can be explained by an overlap of the current with the historic (Pleistocene) refugia of the species. Most likely, the massive recent range loss mainly affected the range which was occupied by rapid post-glacial dispersal. We conclude that massive range losses do not necessarily coincide with genetic impoverishment and that a species' history must be considered when estimating loss of genetic diversity. The assessment of spatial genetic structures and prior phylogeographic information seems essential to conserve once widespread species

Former (light) and present (dark) distribution of <i>P. longicauda</i>.

<p>Approximate collecting locality of the historic Rhine specimens is marked with a star. Subset: collection sites of extant specimens, numbered according to <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031872#pone.0031872.s001" target="_blank">Table S1</a>. The former distribution range of the species was reconstructed after <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031872#pone.0031872-Russev1" target="_blank">[19]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031872#pone.0031872-Andrikovics1" target="_blank">[20]</a>.</p

Relationships of <i>P. longicauda</i> haplotypes.

<p>A – median-joining networks of combined mtCOI and 16S haplotypes of successfully amplified extant specimens. B – median-joining networks of short mtCOI haplotypes of all extant and 24 historic specimens (Körös, Tisza, Maros and Bodrog marked as belonging to the Tisza catchment). Each circle represents a haloptype. The size of the circle indicates the frequency of the haplotype. Connecting lines represent single nucleotide substitutions.</p

Likelihood of ongoing migrations and the timing of the disjunction between the Tisza and Rába catchments.

<p>A – The likelihood of ongoing migration to any directions is 0 (orange: migration from the Tisza to the Rába; blue: migration from the Rába to the Tisza). B – The complete separation of the Tisza and Rába populations most probably happened in the past. An extant connection between the two populations is unlikely.</p

Long-tailed mayfly – <i>Palingenia longicauda</i>.

<p>A – freshly emerged Long-tailed mayfly (photo: A. Móra); B – males surrounding a female in a characteristic flower-like structure (“tiszavirág”) (photo: A. Orosz); C – the synchronized sunset swarming of millions of imagines (photo: L. Polyák).</p

Demographic changes of <i>P. longicauda</i> populations.

<p>The black line shows the mean population size, estimated by Bayesian skyline plot. Grey lines show population sizes within the highest and lowest 95% probability density intervals.</p