Global biogeography of Tetragnatha spiders reveals multiple colonization of the Caribbean

Abstract

Organismal variation in dispersal ability can directly affect levels of gene flow amongst populations, therefore importantly shaping species distributions and species richness patterns. The intermediate dispersal model of biogeography (IDM) predicts that in island systems, species diversity of those lineages with an intermediate dispersal potential is the highest. We broadly test this prediction, focusing on 'four-jawed spiders' (genus Tetragnatha) of the Caribbean archipelago. First, we report on original sampling of this globally distributed genus with numerous widespread as well as endemic species. We then reconstruct multiple Tetragnatha phylogenies from roughly 300 individuals delineated into 54 putative species. Our results support the monophyly of the four-jawed spiders but reject the monophyly of those lineages that reach the Caribbean, where we find low levels of endemism yet high diversity within Tetragnatha. The chronogram detects a potential early overwater colonization of the Caribbean, and in combination with reconstructed biogeographic history, refutes the possibility of ancient vicariant origins of Caribbean Tetragnatha as well as the GAARlandia landbridge scenario. Instead, biogeographic results hypothesize multiple colonization events to, and from the Caribbean since mid-Eocene to late-Miocene. Tetragnatha seems unique among the arachnids explored so far in comprising some species that are excellent dispersers, and others that are not, perhaps having secondarily lost this dispersal propensity. A direct test of the IDM would require consideration of three categories of dispersers. However, four-jawed spiders do not fit one of these three a priori definitions, but rather represent a more complex combination of attributes of a 'dynamic disperser'.

Machine learning approaches identify male body size as the most accurate predictor of species richness

“…Many spider species with high dispersal abilities use ballooning to travel across large distances and to colonize remote islands [37,63,83,84]. While prior works suggest that dispersal ability may shape biodiversity [8,33,35,[85][86][87], our results indicate that it cannot accurately predict species richness. However, the alternative is that the ballooning behavior per se is not a good proxy for organismal dispersal ability.…”

“…Variation in species richness among lineages of comparable taxonomic ranks is often studied locally or within an island system [6,7]. The often detected discrepant patterns are primarily explained by variation in organismal dispersal ability [8,9], niche preemption [10], habitat complexity [11], and the time since a given lineage has occupied the studied area [12]. On the other hand, the identification of attributes impacting large-scale species richness variation, and the extent of its effect, remains opaque and would require more complex approaches [13,14].…”

“…Similarly, phylogenetically older clades are sometimes linked with higher biodiversity due to longer time available for speciation ( [29][30][31] but see [3,32]). Dispersal abilities and intrinsic lineage tendencies for speciation have a notable effect on the creation of discrepancies in species richness among genera or other comparable taxonomic ranks [8,33,34]. The effect of the dispersal ability of a given lineage on its species richness, however, is most likely not linear [9,35].…”

Caribbean golden orbweaving spiders maintain gene flow with North America

“…Trichonephila clavipes resembles the Caribbean pattern detected in the araneid Argiope argentata where island populations clearly interbreed (Agnarsson et al, ). At a higher taxonomic level and within the area of interest, the Caribbean Trichonephila contrasts the two tetragnathid lineages: Cyrtognatha is a relatively poor to intermediate disperser with significant species richness and high endemism, Tetragnatha is a dynamic disperser, with species apparently ranging from extremely good to relatively poor, and shows a high species richness and a mixed endemic to widespread mix of species (Čandek et al, , ). As we show in this study, Trichonephila is an excellent disperser with a single species over the archipelago, exhibiting little genetic structure.…”

“…This has rarely been done, as studies testing the IDM have mainly focused on either only excellent dispersers (Claramunt et al, ) or poor dispersers (Pabijan, Wollenberg, & Vences, ), on laboratory‐reared organisms (Venail et al, ), or they included multiple lineages of incomparable taxonomic ranks (Agnarsson et al, ). In this vein, our prior work has compared a tetragnathid spider lineage with a hypothetical low dispersal potential ( Cyrtognatha ; Čandek et al, ) with its close relative ( Tetragnatha ; Čandek, Agnarsson, Binford, & Kuntner, ) over the Caribbean and the mainland. We found Tetragnatha to be extremely species‐rich in the Caribbean and attributed this richness to a biology that has elements of excellent dispersal, mixed with repeated secondary loss of dispersal ability, all this resulting in a mixed pattern of cosmopolitan, as well as narrowly endemic lineages.…”