Flowing Round the World: Water Snakes (Natricidae) Show Habitat-Related Adaptive Radiation After Dispersal to the New World

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

The manuscript provides sufficient information about the study system, and it adequately cites relevant studies. The goals and methods are clearly described, and the conclusions are supported by the data. However, some sections need further clarification. Below, I provide suggestions that I hope will help the authors improve their manuscript.

First, I suggest citing a reference for the family-level rank Natricidae (as opposed to considering Natricinae as a subfamily of Colubridae). I believe the most recent phylogenetic study that considered the family-level rank Natricidae is by Zaher et al. 2019 (https://doi.org/10.1371/journal.pone.0216148). It’s important to clarify this because the subfamily-level rank Natricinae is also recognized by many researchers/sources, including the Reptile Database (2025).

One of the goals of the study was to examine the rates of evolution of ecologically important traits including body size, diet, and habitat. The authors mention that both diet and habitat appear to exhibit low phylogenetic signal (lines 165-167) and cite a study by Deepak et al. 2022 ("Multilocus phylogeny, natural history traits and classification of natricine snakes"). Did Deepak et al. 2022 test for phylogenetic signal? Please clarify.

The strategy used to analyze the categorical traits, namely by splitting the phylogeny into two separate trees (New World and Old World) is a good way to test if dispersal resulted in increased evolutionary rate.

The first paragraph of the results section focuses on the historical biogeographic analysis, including different dispersal scenarios, but supporting data were not included or mentioned (e.g., map, table, figure, supplementary material). Please provide more details and refer to a map, figure, etc. to support the narrative.

The results show a sharp increase in speciation rate at the root of the New World clade (Fig. 1), which is linked to increases in speciation, extinction, and net diversification rates for all natricids combined. It is worth noting the lack of extinction rate in the Old World natricids (Fig. 2). How realistic is that? Does it mean that no natricid lineages have gone extinct over the past 15+ MY? Please clarify.

In the discussion, the authors argued that habitat shifts (from terrestrial to aquatic environments) followed by fine diet shifts in the aquatic environments are linked to the adaptive radiation of New World natricids—suggesting that there is hierarchical order of differentiation across niches. I suggest the inclusion of a few examples of fine diet shifts in New World natricids to provide some context of the types of changes (e.g., prey type and size, changes in feeding behavior, structural changes in the skull, etc.).

Minor corrections

Line 176: “Body mass data was obtained…” – change to “Body mass data were obtained…” (data is a plural noun)

Overall, I think this is a well-designed study that contributes to the knowledge of diversification of water snakes in the New World.

Author Response

Please see attachment.

Author Response File: Author Response.pdf

Reviewer 2 Report

Comments and Suggestions for Authors

Despite the lack of a broad-scale phylogeny, recent molecular studies have provided phylogenetic estimates for many major groups, including the Natricinae. Of particular interest is the New World group of genera, with high taxonomic diversity of genera and species. The reasons for this broad adaptive radiation are poorly understood, especially given the Asian origin of the Natricinae group. The transition to viviparity is presumably one of the factors that stimulated the divergence of this group in the New World. The study is relevant and will be of interest.

 

Notes:

1. In the Introduction

Lines 93-103: «Analysis of diversification dynamics within Natricidae have recovered an increased speciation rate which coincides with the origin of the New World clade [32]. The origin of viviparity at the root of the New World clade was proposed as a possible key innovation which led to the burst of speciation [32], but this was not explicitly tested due to the lack of variation available (i.e. all New World natricids are viviparous and almost all Old World species are oviparous). Hence, this group of snakes appear to represent a radiation resulting from dispersal to a new continent, but there is currently less evidence available on the question of whether this is an adaptive or non-adaptive radiation. However, an analysis of global snake diets found that the rate of diet evolution is much higher in New World natricids compared to their Old World counterparts [36], suggesting that this may be an important factor."

In the "Discussion" section

Lines 408-412: “Summarizing what we now know, we consider that there is strong evidence for the New World clade of Natricidae as an adaptive radiation, and we hypothesize the following scenario. Evolution of viviparity facilitated the dispersal across the relatively high latitude Beringia land bridge ~15 mya, as this trait is associated with lower temperature tolerance in reptiles (notwithstanding that Beringia was warmer then than it is today) [32,66]."

 

In the work it is necessary to note how the factor of viviparity is consistent with the results and conclusions of this study. For example, the genus Erythrolamprus Wagler, 1830 includes about 50 species that are oviparous, inhabiting humid tropical forests.

 

2. Lines 68-73: "Such non-adaptive radiations may be associated with divergence via barriers to gene flow that result in allopatric speciation under similar environmental conditions, the evolution of sexually selected characters such as ornaments, or coevolutionary processes such as host-parasite cospeciation or arms race coevolution [27,30], which provide alternative explanations for radiations with no discernable link to increased ecological diversity." Most studies note a relative decrease in taxonomic diversity from speciation centers, as well as refugia, which do not always coincide, but are characterized by a high level of endemicity. Also, a high level of helminth diversity is noted for these areas. Also, according to the “Fahrenholz rule”, the phylogeny of parasites reflects the phylogeny of the hosts (Fahrenholz 1913), and host orders or families with high taxonomic differentiation and species richness have a richer and more diverse parasite fauna (Eichler 1948). It is necessary to provide information on the diversity of parasites and pathogens, taking into account the hypothesis of “island” adaptive radiations (which are along trophic axes). There may be discrepancies in the composition and resistance to pathogens.

 

3. Lines 425-433: “Schenk and Steppan [25] discuss in detail the implications of geographic structure and the ability of organisms to disperse across areas for adaptive radiation. Their emphasis on the combination of dispersal across an area to new regions, and adaptation to newly encountered habitats/environments as they spread, is consistent with our results. Moreover, this spatial aspect of adaptive radiation may help explain the rough division of adaptive radiations highlighted in the introduction; namely, that of spatially-constrained ‘island’ radiations differentiated primarily by trophic ecology vs less spatially-constrained ‘continental’ radiations primarily differentiated by habitat. Specifically, continental radiations may have sufficient space to continue dispersing and encountering new environments which will facilitate continued adaptation to these over a longer period (Fig. 5).»

 

To support the hypothesis of «island’ radiations» it is also necessary to take into account paleontological data, data on the diversity of helminths, and invasion processes on the island of Mallorca, for example, Natrix maura (Linnaeus, 1758) on the island of Mallorca (Kraus, 2015, doi: 10.1146/annurev-ecolsys-112414-05445).

 

Reference:

Kraus, F. Impacts from Invasive Reptiles and Amphibians. Annual Review of Ecology, Evolution, and Systematics 2015, 46(1), 75-97.

Author Response

Please see attachment.

Author Response File: Author Response.pdf