Inferring species trees from gene trees in a radiation of California trapdoor spiders (Araneae, Antrodiaetidae, Aliatypus)

Abstract

Background: The California Floristic Province is a biodiversity hotspot, reflecting a complex geologic history, strong selective gradients, and a heterogeneous landscape. These factors have led to high endemic diversity across many lifeforms within this region, including the richest diversity of mygalomorph spiders (tarantulas, trapdoor spiders, and kin) in North America. The trapdoor spider genus Aliatypus encompasses twelve described species, eleven of which are endemic to California. Several Aliatypus species show disjunct distributional patterns in California (some are found on both sides of the vast Central Valley), and the genus as a whole occupies an impressive variety of habitats.

Methodology/principal findings: We collected specimens from 89 populations representing all described species. DNA sequence data were collected from seven gene regions, including two newly developed for spider systematics. Bayesian inference (in individual gene tree and species tree approaches) recovered a general "3 clade" structure for the genus (A. gulosus, californicus group, erebus group), with three other phylogenetically isolated species differing slightly in position across different phylogenetic analyses. Because of extremely high intraspecific divergences in mitochondrial COI sequences, the relatively slowly evolving 28S rRNA gene was found to be more useful than mitochondrial data for identification of morphologically indistinguishable immatures. For multiple species spanning the Central Valley, explicit hypothesis testing suggests a lack of monophyly for regional populations (e.g., western Coast Range populations). Phylogenetic evidence clearly shows that syntopy is restricted to distant phylogenetic relatives, consistent with ecological niche conservatism.

Conclusions/significance: This study provides fundamental insight into a radiation of trapdoor spiders found in the biodiversity hotspot of California. Species relationships are clarified and undescribed lineages are discovered, with more geographic sampling likely to lead to additional species diversity. These dispersal-limited taxa provide novel insight into the biogeography and Earth history processes of California.

Figure 1. Map of California showing sampling localities, with colors corresponding to species (see insert).

Sites with species syntopy highlighted with a white circle (27: A. trophonius & A. californicus; 30, 36, 41: A. californicus & A. erebus; 47: A californicus & erebus group immature). Black text designates locations where immature specimens could not be confidently identified. Detailed collection information can be found in Table S1.

Figure 2. 28S Bayesian phylogram.

Posterior probabilities shown for all major clades. Taxon names consist of species, MY (or GMY) number, and collecting locality (see Fig. 1). Immature specimens are denoted with imm; western localities for transvalley taxa denoted with black dots.

Figure 3. COI Bayesian phylogram.

Posterior probabilities shown for all major clades. Taxon names consist of species, MY (or GMY) number, and collecting locality (see Fig. 1). Immature specimens are denoted with imm; western localities for transvalley taxa denoted with black dots. Taxon names in black are immatures that could not be confidently identified. Insert image of an adult female Aliatypus thompsoni from the central Transverse Ranges (Ventura Co., Cerro Noroeste Road).

Figure 4. Bayesian phylograms from 18S rRNA, Hsp70 nDNA, Fox-D nDNA, EF-1γ nDNA, and Wingless nDNA matrices.

Asterisks indicate pp values above 0.95%. The californicus and erebus group species are indicated by colored branches (see insert). Outgroups have been removed from gene trees for illustration purposes.

Figure 5. Species trees estimated with concatenation and coalescent approaches.

Panel A: Bayesian phylogram of concatenated matrix; posterior probabilities shown for all nodes. Panel B: Phylogeny estimated with *BEAST; posterior probabilities shown for all nodes. Patterns of syntopy displayed for Aliatypus, corresponding to Table 3. Outgroups have been removed from species trees for illustration purposes.