Evolutionary history of the endemic water shrew Neomys anomalus: Recurrent phylogeographic patterns in semi‐aquatic mammals of the Iberian Peninsula

Abstract

The Cabrera's water shrew (Neomys anomalus) is a small semi‐aquatic mammal whose taxonomic status was recently elevated from subspecies to species; as a consequence of this change, this species is now endemic to the Iberian Peninsula. In this study, we looked at its evolutionary history by combining phylogeography, the spatial distribution of genetic diversity, and species distribution modeling. To perform these analyses, we used noninvasive samples collected across the species distribution range and sequenced partial mitochondrial cytochrome b and D‐loop genes. Maximum‐likelihood and Bayesian phylogenetic trees derived from these sequences indicated that N. anomalus is divided into two main phylogroups that correlate strongly with geography, with two contact zones between the groups that showed limited spatial mixing between them. River basins were responsible for only a small percentage of the structure of the genetic diversity of this species despite its riparian habitat. The nucleotide diversity variation map showed the highest genetic diversity to be in the north of the Iberian Peninsula. Finally, species distribution modeling allowed the inference of an optimal area during the Last Interglacial in the north of the Iberian Peninsula, and multiple glacial refugia during the Last Glacial Maximum. The phylogeographic pattern of N. anomalus is strikingly similar to that of another semi‐aquatic Iberian mammal, the Pyrenean desman (Galemys pyrenaicus), revealing how Pleistocene glaciations could have had equivalent effects on species of similar ecology and distribution. This phylogeographic structure is consistent with N. anomalus having been isolated for long periods in multiple glacial refugia within the Iberian Peninsula, in agreement with the “refugia‐within‐refugia” hypothesis, and further supporting its status as a distinct species.

Comparative phylogeography of mainland and insular species of Neotropical molossid bats (Molossus)

“…Evolutionary geographic patterns and demographic histories of species are largely affected by historical events, habitat preferences, and geographic barriers (Bernatchez & Wilson, ; Querejeta & Castresana, ; Soltis, Morris, McLachlan, Manos, & Soltis, ). Moreover, several mechanisms might result in genetic isolation, such as geography and ecology, which often interact to shape the current pattern of diversity, but also making it difficult to distinguish the primary diversification factors (Wang & Bradburd, ).…”

Size increase without genetic divergence in the Eurasian water shrew Neomys fodiens

“…This size increase in a specific population is striking, as the morphology of this species is fairly stable across the rest of its European range 20 . N. f. niethammeri lives sympatrically with N. anomalus 21 , which was recently separated from the European species N. milleri 13,22 . A population of the nominal subspecies N. f. fodiens is found beyond the range of N. f. niethammeri 12 , making that the population of N. f. niethammeri is flanked by populations of N. f. fodiens (Supplementary Fig.…”

“…Improved laboratory techniques, many adopted from ancient DNA studies that target low quality and degraded DNA, have enabled the use of non-invasive and minimally invasive samples as well as different types of post mortem remains in phylogeographic studies 26,27 . This has made it possible to genetically analyze elusive and threatened species, as larger sample sets that do not require the manipulation or capture of specimens become available for study 22,28,29 . For example, skull bones obtained from owl pellets containing undigested material from small mammal prey have been used in various phylogeographic studies 30–32 .…”

Ecological and phenotypic divergence in Iberian shrews (Soricidae)

“…and Neomys anomalus, which shows a patchy geographic range and has been recently separated from its sister species of European distribution N. milleri (Mottaz 1907) (see Castiglia, Annesi, Aloise, & Amori, 2007;Igea, Aymerich, Bannikova, Gosálbez, & Castresana, 2015;Querejeta & Castresana, 2018). Thus, both species the Iberian endemism N. anomalus and its Palearctic counterpart N. milleri have now species status as originally described (Cabrera 1907, Mottaz 1907).…”

“…Nine soricid species representing two subfamilies, white‐toothed (Crocidurinae) and red‐toothed shrews (Soricinae), and four genera ( Sorex , Crocidura , Neomys, and Suncus ) inhabit the Iberian Peninsula: the common or Eurasian shrew ( Sorex araneus Linnaeus 1758), that is widely distributed in the Palaearctic; Sorex granarius , endemic to the Iberian Peninsula; the crowned shrew or Millet's shrew ( Sorex coronatus Millet 1928), which occurs from northern Spain (Pyrenees) throughout France and the Low Countries, to northern Switzerland and Germany; the Eurasian Pygmy Shrew ( Sorex minutus Linnaeus 1776), which shows a disjunct distribution in the Iberian Peninsula with isolated populations in Sistema Central (Sierra de Gredos and Guadarrama mountain ranges) and Northeastern Spain (Tarragona province); the white‐toothed shrew ( C. russula ), the most common shrew in Spain and widely distributed throughout southern and western Europe; the lesser white‐toothed shrew ( Crocidura suaveolens Pallas 1811), which occurs at much lower densities than its congener C. russula in the western part of its range where is relatively uncommon; the Etruscan shrew ( Suncus etruscus Savi 1822), the smallest known mammal (<2 g), whose distribution in Europe is confined to the Mediterranean climate zone; the Eurasian water shrew ( Neomys fodiens Pennant 1771), an abundant species throughout the Palearctic and the largest (15–20 g) of the soricids inhabiting Iberia; and Neomys anomalus , which shows a patchy geographic range and has been recently separated from its sister species of European distribution N. milleri (Mottaz 1907) (see Castiglia, Annesi, Aloise, & Amori, ; Igea, Aymerich, Bannikova, Gosálbez, & Castresana, ; Querejeta & Castresana, ). Thus, both species the Iberian endemism N. anomalus and its Palearctic counterpart N. milleri have now species status as originally described (Cabrera 1907, Mottaz 1907).…”