Rate heterogeneity across Squamata, misleading ancestral state reconstruction and the importance of proper null model specification

Abstract

The binary-state speciation and extinction (BiSSE) model has been used in many instances to identify state-dependent diversification and reconstruct ancestral states. However, recent studies have shown that the standard procedure of comparing the fit of the BiSSE model to constant-rate birth-death models often inappropriately favours the BiSSE model when diversification rates vary in a state-independent fashion. The newly developed HiSSE model enables researchers to identify state-dependent diversification rates while accounting for state-independent diversification at the same time. The HiSSE model also allows researchers to test state-dependent models against appropriate state-independent null models that have the same number of parameters as the state-dependent models being tested. We reanalyse two data sets that originally used BiSSE to reconstruct ancestral states within squamate reptiles and reached surprising conclusions regarding the evolution of toepads within Gekkota and viviparity across Squamata. We used this new method to demonstrate that there are many shifts in diversification rates across squamates. We then fit various HiSSE submodels and null models to the state and phylogenetic data and reconstructed states under these models. We found that there is no single, consistent signal for state-dependent diversification associated with toepads in gekkotans or viviparity across all squamates. Our reconstructions show limited support for the recently proposed hypotheses that toepads evolved multiple times independently in Gekkota and that transitions from viviparity to oviparity are common in Squamata. Our results highlight the importance of considering an adequate pool of models and null models when estimating diversification rate parameters and reconstructing ancestral states.

How mountains shape biodiversity: The role of the Andes in biogeography, diversification, and reproductive biology in South America's most species‐rich lizard radiation (Squamata: Liolaemidae)

“…Reanalyses of these data have produced more conservative results, showing much fewer reversals (King and Lee ; Wright et al. ; Harrington and Reeder ). Nevertheless, these results still support previously identified reversals, including sand boas ( Eryx ) (Lynch and Wagner ) and bushmaster vipers ( Lachesis ) (Fenwick et al.…”

Tempo and mode of performance evolution across multiple independent origins of adhesive toe pads in lizards

“…Gamble et al (2012) found toe pads to be associated with slightly higher rate of diversification, although this was not the case for Garcia-Porta and Ord (2013). Considering state-correlated diversification rate alongside an ancestral state reconstruction, Harrington and Reeder (2017) concluded a single origin of toe pads using a "hidden states" binary-state speciation and extinction model (Maddison et al 2007;Beaulieu et al 2013;Beaulieu and O'Meara 2016), although Gamble et al (2017) dispute these results due to potentially high Type 1 error rates (Davis et al 2013;Maddison and FitzJohn 2015;Rabosky and Goldberg 2015). Future studies may want to consider incorporating character-state correlated diversification information into ancestral state reconstructions using the recently published nonparametric FiSSE (Fast, intuitive, State-dependent, Speciation-Extinction) approach (Rabosky and Goldberg 2017;Zenil-Ferguson and Pennell 2017).…”

Multiple origins of sexual dichromatism and aposematism within large carpenter bees

“…Similarly, in diving beetles of the genus Exocelina, a rate shift was recovered and connected to the colonization of a new biogeographic region (Toussaint et al 2015). In previous cases, where both BAMM and HiSSE models have been used side by side, diversification rates and estimated shifts usually agree (Harrington and Reeder 2017;Sahoo et al 2017). It is difficult to discern which method provides the more credible result for diversification rates within Xylocopa -HiSSE that estimated an increased diversification rate for the dichromatic clades, or BAMM that showed no shifts in diversification.…”

“…We compared 16 models of diversification and trait evolution in the HiSSE framework (Table 1), using guidelines and code provided by a study assessing the diversification of Squamates (Harrington and Reeder 2017). We implemented six character-independent null models, CID-2 and CID-4 models (sensu Beaulieu and O'Meara 2016); included among these is an extension of the currently implemented CID-4 models in the HiSSE package that allows for nine transition rates, as proposed by Harrington and Reeder (2017). Three models excluded hidden states and are therefore considered "BiSSE-like."…”

“…Essentially, we tested the fit of our data to the full HiSSE model, and six subsets hereof with various constraints on transition and diversification rates. Refer to Beaulieu and O'Meara (2016) and Harrington and Reeder (2017) for a more extensive description of the tested models. We implemented six character-independent null models, CID-2 and CID-4 models (sensu Beaulieu and O'Meara 2016); included among these is an extension of the currently implemented CID-4 models in the HiSSE package that allows for nine transition rates, as proposed by Harrington and Reeder (2017).…”