How important is it to consider lineage diversification heterogeneity in macroevolutionary studies? Lessons from the lizard family Liolaemidae

Abstract

Macroevolutionary and biogeographical studies commonly apply multiple models to test state-dependent diversification. These models track the association between states of interest along a phylogeny, although many of them do not consider whether different clades might be evolving under different evolutionary drivers. Yet, they are still commonly applied to empirical studies without careful consideration of possible lineage diversification heterogeneity along the phylogenetic tree. A recent biogeographic study has suggested that orogenic uplift of the southern Andes has acted as a species pump, driving diversification of the lizard family Liolaemidae (307 described species), native to temperate southern South America. Here, we argue against the Andean uplift as main driver of evolution in this group. We show that there is a clear pattern of heterogeneous diversification in the Liolaemidae, which biases state-and environment-dependent analyses in, respectively, the GeoSSE and RPANDA programs. We show here that there are two shifts to accelerated speciation rates involving two clades that have both been classified as having "Andean" distributions. We incorporated the Geographic Hidden-State Speciation and Extinction model (GeoHiSSE) to accommodate unrelated diversification shifts, and also re-analyzed the data in RPANDA program after splitting biologically distinct clades for separate analyses, as well as including a more appropriate set of models. We demonstrate that the "Andean uplift" hypothesis is not supported when the heterogeneous diversification histories among these lizards is considered. We use the Liolaemidae as an ideal system to demonstrate potential risks of ignoring clade-specific differences in diversification patterns in macroevolutionary studies. We also implemented simulations to show that, in agreement with previous findings, the HiSSE approach can effectively and substantially reduce the level of distribution-dependent models receiving the highest AIC weights in such scenarios. However, we still find a relatively high rate (15%) of distribution-dependent models receiving the highest AIC weights, and provide recommendations related to the set of models included in the analyses that reduce these rates by half. Finally, we demonstrate that trees including clades following different dependent-drivers affect RPANDA analyses by producing different outcomes, ranging from partially correct models to completely misleading results. We provide recommendations for the implementation of both programs.

Looking at the past to infer into the future: Thermal traits track environmental change in Liolaemidae*

“…The diversification of Liolaemidae is an outcome of historical biogeography (Olave et al. 2020), and evolutionarily labile thermal physiology, but this is more remarkable in Liolaemus , because trait evolution has been more conservative in Phymaturus and Ctenoblepharys .…”

Evolutionary transitions in diet influence the exceptional diversification of a lizard adaptive radiation

“…However, in this study, high extinction rates in Phymaturus rank this group second in net diversification rate [ 44 ]. This may be related to the fact that this genus is dominated by strong niche conservatism with species sharing multiple key ecological and life history traits, including their adaptation to cold climates, their occupation of rocky outcrops, their herbivorous diets, viviparous reproductions, and extreme low fecundity [ 26 , 46 , 49 , 53 , 54 ]. Conversely, herbivory in Liolaemus unlike Phymaturus evolved convergently (nine times), and in all cases the insectivore ancestor had to undergo an omnivorous transition; thus, it is likely that the common ancestor of both Phymaturus and Liolaemus was probably an omnivore.…”

“…One possibility is that some traits allow the use of resources more efficiently, triggering species diversification [ 45 ]. For instance, dietary niches might be a key factor driving species diversification [ 17 – 19 ], helping to explain the extreme variation in both diversification rates and dietary niches in the liolaemid family, especially if the effect of other possible traits such as habitat or parity mode is ruled out [ 46 , 47 ].…”

Male genitalia's evolutionary rate is higher than those of body traits: the case of two Liolaemus lizards' group

“…The low divergence in genital morphology in the L. elongatus group could explain the hybridization processes between sympatric species, as was hypothesized by Troncoso‐Palacios et al (2019). Although is important to mention that in general L. elongatus group exhibits highly evolutionary patterns (Olave et al ., 2020).…”