Ephemeral-habitat colonization and neotropical species richness of Caenorhabditis nematodes

Abstract

BackgroundThe drivers of species co-existence in local communities are especially enigmatic for assemblages of morphologically cryptic species. Here we characterize the colonization dynamics and abundance of nine species of Caenorhabditis nematodes in neotropical French Guiana, the most speciose known assemblage of this genus, with resource use overlap and notoriously similar external morphology despite deep genomic divergence.MethodsTo characterize the dynamics and specificity of colonization and exploitation of ephemeral resource patches, we conducted manipulative field experiments and the largest sampling effort to date for Caenorhabditis outside of Europe. This effort provides the first in-depth quantitative analysis of substrate specificity for Caenorhabditis in natural, unperturbed habitats.ResultsWe amassed a total of 626 strain isolates from nine species of Caenorhabditis among 2865 substrate samples. With the two new species described here (C. astrocarya and C. dolens), we estimate that our sampling procedures will discover few additional species of these microbivorous animals in this tropical rainforest system. We demonstrate experimentally that the two most prevalent species (C. nouraguensis and C. tropicalis) rapidly colonize fresh resource patches, whereas at least one rarer species shows specialist micro-habitat fidelity.ConclusionDespite the potential to colonize rapidly, these ephemeral patchy resources of rotting fruits and flowers are likely to often remain uncolonized by Caenorhabditis prior to their complete decay, implying dispersal-limited resource exploitation. We hypothesize that a combination of rapid colonization, high ephemerality of resource patches, and species heterogeneity in degree of specialization on micro-habitats and life histories enables a dynamic co-existence of so many morphologically cryptic species of Caenorhabditis.Electronic supplementary materialThe online version of this article (10.1186/s12898-017-0150-z) contains supplementary material, which is available to authorized users.

X exceptionalism in Caenorhabditis speciation

“…Despite widespread geographic distributions for many species of Caenorhabditis , no examples of clinal trait variation or hybrid zones are known. Tropical regions are most speciose and so offer the greatest opportunity for sympatry of closely related species (Cutter, ; Felix et al., ; Ferrari et al., ; Kiontke et al., ). Given that many species are known from just a single sampling location, often on islands (Cutter, ; Kiontke et al., ), it remains to be determined how crucial is geographic isolation in allopatry and to what extent sex chromosome evolution plays into the evolution of reproductive isolation upon secondary contact.…”

“…The sex determination system of C. elegans can be manipulated genetically to change the XO chromosomal system to create neo-sex chromosomes to mimic XY, ZW or environmental sex determination systems (Chandler, Chadderdon, Phillips, Dworkin, & Janzen, 2012;Hodgkin, 2002). Similar approaches should be feasible in other species (Haag & Liu, 2013 Tropical regions are most speciose and so offer the greatest opportunity for sympatry of closely related species (Cutter, 2015;Felix et al, 2013;Ferrari et al, 2017;Kiontke et al, 2011). Given that many species are known from just a single sampling location, often on islands (Cutter, 2015;Kiontke et al, 2011), it remains to be determined how crucial is geographic isolation in allopatry and to what extent sex chromosome evolution plays into the evolution of reproductive isolation upon secondary contact.…”

Comparative genomics of 10 newCaenorhabditisspecies

“…; Ferrari et al. ). This new understanding, combined with extensive worldwide sampling efforts, has led to the discovery of more than 50 species (Kiontke et al.…”

“…; Ferrari et al. ; MAF, LF, MVR, CB, unpublished; John Wang, Michael Ailion, Erik Andersen, Asher Cutter, pers. comm.)…”

“…The discovery of new Caenorhabditis species was, for many years, hindered by a poor understanding of the natural ecology of these nematodes (Félix & Braendle 2010). Surveys of natural populations of C. elegans and Caenorhabditis briggsae revealed that, rather than being "soil nematodes," Caenorhabditis species thrive in microbe-rich environments, such as rotting fruits, flowers, and stems (Kiontke et al 2011;Félix & Duveau 2012;Félix et al 2014;Ferrari et al 2017). This new understanding, combined with extensive worldwide sampling efforts, has led to the discovery of more than 50 species (Kiontke et al 2011;Félix et al 2014;Ferrari et al 2017;MAF, LF, MVR, CB, unpublished;John Wang, Michael Ailion, Erik Andersen, Asher Cutter, pers.…”