Peer review of: The evolution of parental care diversity in amphibians (2019)

Reviewers' Comments:  
 
Reviewer #1:  
Remarks to the Author:  
Overall, I found this to be an important and interesting study well-worth publishing. While other 
studies of the evolution of parental care and reproductive strategies in amphibians have been done, 
this is the most extensive one that I know of. The authors have accumulated an impressive dataset 
that will, I think, be useful to comparative evolutionary biologists for years to come. Beyond this, the 
authors have been able to focus on what (in my opinion) are interesting questions that have not been 
adequately addressed in a comparative framework. The idea that simple characters should evolve 
more rapidly and be more volatile than complex characters is a concept of general interest in 
evolutionary biology, and the authors are able to address this issue in a convincing manner with their 
dataset. The stability of biparental care is another issue of general interest to both theoreticians and 
empiricists, and the authors of this study are able to provide some novel insights in this regard. The 
methods used are current, and appear appropriate to the questions they were used to address. I had 
just a few minor comments that should be addressed before publication, as noted below.  
 
Line 67: The claim that behaviors that cannot easily classified as simple or complex should evolve at 
intermediate rates seems somewhat vague. I think it might be worth specifying exactly which 
behaviors those are, and making a specific case for each one.  
 
Line 187: I would be curious to know if the results remain (qualitatively) the same if behaviors (like 
viviparity) that span early to late stages were classified as later (I think a case could be made that this 
would be a logical category for that type of behavior).  
 
Line 370: Change "allows to reduce model complexity and over-parametrization" to "enables a 
reduction of model complexity and over-parametrization"  
 
 
 
Reviewer #2:  
Remarks to the Author:  
In this paper Furness and Capellini report on evidence of parental care across over 1000 species of 
amphibians about 40% of which have been recorded as displaying some form of parental care. They 
use this data set to carry out several phylogenetic comparative analyses to elucidate the origins and 
evolutionary diversification of parental care. Specifically, they focus on three main hypotheses, a) that 
simple forms of parental care are more evolutionary labile than complex forms of parental care, b) 
that care during the early stages of juvenile development is a precursor for care at later stages of 
juvenile development and b) that biparental care will exhibit greater evolutionary stability when 
parents vary in what form of care they exhibit. They find some support for the first two hypotheses 
but limited support for the last hypothesis.  
 
Overall this is an impressive data set that has the potential to contribute to our growing understanding 
of the origins and evolution of parental care. Amphibians are particularly tractable systems for 
exploring these questions because of the considerable diversity of parental care exhibited 
(functionally, taxonomically and in terms of which sex provides the care) providing opportunities to 
develop and test clear hypotheses above the factors responsible for that variation. The paper goes 
some way to addressing some of these questions and will no doubt provide a basis from which future 
hypothesis driven tests of the mechanisms underpinning some of the patterns elucidated could be 
undertaken. However, I had several questions regarding the conceptual basis of the paper that I think 
need to be addressed before the paper can really deliver on its promise. Furthermore, there are 

several key aspects of the analysis that need to be addressed before the results can be interpreted 
with confidence. Below I detail these concerns.  
 
Major Comments  
 
My major comment regards the overall conceptual framework from the paper with respect to the 
specific aim of understanding patterns underlying the origins and evolution of parental care. This is a 
substantial challenge and one which the amphibian data set is potentially well established to test – 
however, I am not sure the framework of your paper is really set up appropriately to explore this 
question in the most powerful way possible. The paper at the moment is set up to explore what read 
at time as three disparate aims that are of relevance, broadly, to understanding the evolution of 
parental care. These aims are all interesting and important to address, but I think they probably want 
to be brought together so that the paper has a single narrative to it. At the moment it appears, in 
places, that the paper is there to tick off a number of understudied areas in parental care research 
rather than to use the data to understand evolutionary patterns of parental care in amphibians in a 
holistic manner. To address this I think that the paper could perhaps be split up into three sections – 
the first is understanding the origins and elaboration of care across different life history stages, the 
second is understanding the elaboration of care across functional context within life history stages, 
and the third is a question about the extent to which these differ between males and females and the 
evolution of bi-parental care more broadly. I think this would allow you to provide a more powerful 
and structured analysis of the evolutionary patterns of parental care diversification than you currently 
report. Indeed, at present the initial major focus is on the evolutionary lability of simple vs complex 
traits. This is of course relevant to the data on parental care that has been collected for this paper but 
is perhaps represents a more general question than the one being posited here. Instead I think that 
this aspect of the paper would be better incorporated into a more explicit focus on parental care itself 
where the results in terms of variation in the evolutionary lability of traits emerges as an outcome of 
the models rather than as an explicit focus.  
 
To address these concerns, I would suggest a slight change in overall focus. I think the major focus 
should be on the extent to which simple forms of early parental care (care at the egg stage, viviparity) 
sets the stage for prolonged parental care at the larval and juvenile stage. This is the key question 
that your data allows you to address – given that you do not have predictors for what drives the initial 
emergence of care itself. When doing this, I would also suggest simplifying this analysis somewhat. 
That is, I would first simply ask whether care at the larval/juvenile stage is more likely to evolve from 
a background of egg care/viviparity or no care. To achieve this, I wonder if you need the diversity in 
care types for this initial step and instead just include the presence and absence of care at each of 
those stages. Instead you could focus on a simple framework like this (apologies if this is slightly 
oversimplified):  
 
a) Egg Care -----------> larval Care ------------> Juvenile Care  
b) Egg Care (with direct development ------> Juvenile Care  
c) Viviparity ----------------------------------------> Juvenile Care  
 
You would then be interested in asking very simple questions regarding the extent to which Juvenile 
care evolves as a function of any earlier attendance (e.g., combine a, b and c) or whether this differs 
for the different early stage care backgrounds (separate analyses for a, b and c). This would then 
allow you to not only ask whether parental care at the juvenile stage evolves as a function of parental 
care at earlier stages but also whether the context of that early care matters (similar to the recent 
analysis done for reptiles). You could also do a smaller separate analysis for the extent to which egg 
care predicts larval care.  
 

Combined I think this would provide a more robust analysis of how parental care evolved and the 
extent to which care in the later stages is dependent on care in the early stages (and how that differs 
depending on the nature of that early care). Interestingly, as your data suggests, it would also allow 
you to compare this to instances where the evolution of care in early vs late stages represent 
independent evolutionary events. This would provide a nice framework for a discussion (and 
potentially future analyses) on the factors that might have promoted this (e.g., there is different 
selection on care at the different stages). There are some analogous systems in which these questions 
have been studied. For example, Michael Griesser’s work on the evolution of family living and 
cooperation in birds (PlosBiol 2017).  
 
Importantly, the above approach would also then allow you to explore the question of the extent to 
which parental care elaborates within each of these care types. That is, do more complex forms of 
parental care evolve from simple forms of care. So, within these care types, does egg attendance 
provide a precursor for the evolution of brooding, feeding, transport or do those traits emerge 
independently (although see requirement for clarification on this point below). In this context 
questions about the lability of simple vs complex traits perhaps becomes more relevant as it allows 
you to say something about the evolutionary lability of simple attendance across these different stages 
and then how this has provided the basis from the evolution of further elaboration of care - and how 
that subsequently influences the maintenance of care.  
 
Re-structuring the analysis in this way would also help clarify the role that traits such as vivparity play 
in this process. The complication is that viviparity can be viewed as both an evolved parental care 
strategy as well as a fundamental precursor to greater elaboration of care types. You seem to focus 
largely on the former in this instance (e.g., you state that viviparity is an extended form of parental 
care to occurs across life stages) but the above would allow you to use viviparity more powerfully to 
explore some of the precursors to extended forms of parental care. Indeed, one of the benefits of 
amphibians is that they exhibit multiple parity forms that provide fundamentally different associations 
between mothers and their offspring – which may have implications for the subsequent evolution of 
prolonged care (as well as other traits – as articulated in the introduction).  
 
Minor Points  
 
Introduction  
 
Page 3, Lines 42: Minor point but I would finish the first paragraph here and start a second paragraph 
from “While care behaviours…”. I think this would provide a more powerful introduction to the paper.  
 
Page 3, Lines 43 – 46: This is a long sentence I would consider splitting it in two.  
 
Page 3, Lines 43 – 46: I would also argue that the main reason for this is that in few systems is there 
the requisite diversity of care types to allow for a proper analysis of these traits.  
 
Page 5, Lines 80 – 83: Is there data on these traits in offspring that could be tested in the context of 
the predictors of the loss of different care types? This may be outside the score of the study, but it 
seems to me that this data set may also allow you to explore the extent to which the evolution of 
different care types have resulted in the evolution of offspring traits (perhaps focussing on the 
evolution of increasingly altricial offspring) – which may help explain the lability of different care 
types.  
 
Page 6, Lines 105 – 106: Does this not depend on the sex that has predominantly evolved to care for 
the offspring? For example, in systems where there is predominantly female only care bi-parental care 

occurs when males also stay and help – but the opposite is true of systems in which there is 
predominantly male only care (e.g., some fish). I guess amphibians are interesting in this context as 
they have  
both external and internal fertilisation thus presumably both male and female care can evolve. I 
wonder if this should be incorporated into the analysis?  
 
Page 7, Line 135: Is origin and diversification a better term here than origin and maintenance?  
 
Page 7, lines 139 – 141: Is this not expected given that attendance is necessarily a precursor to the 
other forms of care – that is that attendance must also be present in the context of the other care 
types. Perhaps this is a semantic question. But to me this question is about whether egg attendance 
evolves more readily than egg attendance with brooding/feeding/transport or is the definition of egg 
attendance separate to those other care types? To me this is not at all surprising and it needs to be 
coaxed in with the other results to really maximise its interest. That attendance is a precursor to more 
complex forms of parental care and that parental care in eggs is a precursor (or not) to parental care 
at other juvenile life stages. The fact that attendance is more likely to be lost also makes sense in this 
context, but I am not sure it is the big sell of this paper.  
 
Page 7, Lines 141 – 145: I was confused by this statement. The statement here suggests that the rate 
of loss of tadpole feeding is high (“being high for traits such as tadpole feeding”) – which is supported 
by the data in figure 1c and table S2 – but this then appears at odds with the data presented in figure 
1d which suggested that there is no evidence of an evolutionary loss of tadpole feeding. The opposite 
is true for egg attendance. Am I missing something here?  
 
Page 8, Lines 152 – 154: How relevant is it to collapse the data across functional context. While I can 
appreciate that for a simple trait such as attendance is equivalent – it's a simple increase in 
association between parents and offspring – I am not sure whether this is the case for brooding and or 
transport. This is important because the interpretation here lies in the assumption that the complexity 
of these behaviours is equivalent across life stages – which might not be the case – egg brooding or 
transport for example may be less complex than juvenile transport.  
 
Page 9 and 10, Lines 191 – 192: Here and throughout you report the Log BF outputs of your models 
but for someone not familiar with these models it is difficult to know what a particular LogBF value 
means in terms of effect size. Perhaps this can be made clearer.  
 
Page 9 and 10: Lines 190 – 194: These two sentences appear to directly contradict one another. “We 
find strong support for correlated evolution between early and late care. Parental care at the egg 
stage is equally likely to evolve and revert to no care, as it is to facilitate the evolution of prolonged 
care through the acquisition of care at the later development stage.“ This is then further contradicted 
in Lines 199 – 201 which states that nearly all the evolutionary origins of late care have evolved when 
early care is already present”. Perhaps I have missed something, but I think these statements need to 
be cleared up.  
 
Page 9 and 10: Lines 190 – 194: Does the data also suggest that late care is also just as likely to 
facilitate the evolution of care across both early and late stages (figure 2)? This does not seem to be 
discussed anywhere. Is this a likely scenario in reality?  
 
Page 10, Lines 194 – 196: See comment above but I think this is a neat result that will provide a 
foundation for future work. It suggests that alternative pressures may influence care at different life 
stages and thus it would be interesting to know what they are. As suggested above, there is some 
precedence for this for other social traits.  

 
Page 10, Lines 201 – 203: Ok but would you expect that tadpole feeding per se would be likely to 
have an evolutionary link to parental care at the egg stage beyond the fact that parental care at the 
egg stage may mean that there is more likely to be care at the larval/juvenile stage full stop? As 
detailed above, this suggests to me that you are more broadly interested in the extent to which any 
form of care at the juvenile stage is likely to have been preceded by care at a previous stage. The 
elaboration of care within each stage is then a separate question.  
 
Page 11, Lines 226 – 234: I do not see how this information follows from the previous information 
regarding the evolution of male, female or bi-parental care. Indeed, as you have no information on the 
extent to which the evolution of increase parent-offspring associations and elaboration of care then is 
mediated by, or mediates, levels of conflict within the brood I would suggest dropping these 
discussion points.  
 
Page 12, Lines 240 – 243: As detailed above, it is not clear what you mean by a reduction in the 
duration of care? Does this mean that species can go from caring right across the offspring’s 
developmental period to only one or two stages? If so, I am not sure I can see where that specific 
data is reported. What your data reports is that parental care is just as likely to be last as it is to 
result in more prolonged care (e.g., Figure 2). I think loss of care as opposed to reduced duration I 
perhaps a more appropriate word here.  
 
Page 12, Lines 255 – 257: Again, I am not sure what you mean here by the correlated evolution 
between male and female care. Does this mean that where different care traits evolve they are as 
equally likely to evolve in males compared to females? This seems interesting to me – as detailed 
above, would we not predict that male and female only care would evolve under different scenarios 
based on, for example, fertilisation mode which I presume would have a strong phylogenetic signal. 
The fact that both male only and female only female care evolves under the same phylogenetic 
circumstances makes me wonder what are the circumstances under which one evolves vs the other. Is 
it worth discussing this point?  
 
Page 12 and 13, Lines 260 – 261: Is this not dependent on the extent of variation in fertilisation mode 
which has been suggested to mediate the outcome of sex specific conflict in care? In systems that 
include both male only and female only care then bi-parental care has a greater opportunity to evolve 
from a background of both. This is in contrast to various other terrestrial vertebrates – for example 
mammals and birds – in which females are the primary care givers and therefore the most 
parsimonious (and in many instances only) route to bi-parental care is males joining females. These 
points I think need to be discussed (see also previous point).  
 
Page 13, Lines 261 – 263: Higher rates than what?  
 
Page 13, Lines 263 – 267: It would be nice to have an idea of the number of transitions to and from 
male/female only care and biparental care within these traits so that the reader can interpret the data 
in the context of the statistical power. I could not find the data relating to this anywhere.  
 
Page 13, Lines 279 – 283: Same goes for the data on complementary vs different care types. I also 
wondered how this works? How do you get a system in which males and females perform care 
behaviours at different stages of offspring development? This would require one of the sexes to 
remain in the other sexes home range and not perform any care at one stage but then take over at a 
later stage. What evidence is there that this occurs. Presumably, this must co-occur with other aspects 
of the mating social system.  
 

Page 16, Lines 330 – 333: You state that data from reviews were supplemented with data from the 
primary and secondary literature but don't supply any information on how (I also could not find this in 
the supp info). What searchers were done to complement those studies, what were the search terms 
used, what was the depth of literature searched?  
 
Supp Info, Page 1, Lines 17 – 21: You state that you did not include short term egg attendance (egg 
attendance immediately after birth) but what about egg attendance that did not go throughout the 
entire period. This is important because egg attendance for a prolonged period at the end of the 
developmental period is likely to exert a much more significant effect on the likelihood of post 
hatching care than egg attendance for a prolonged period of time at the begging. What data is there 
out there on duration of attendance and when that attendance occurs?  
 
 
 
Reviewer #3:  
Remarks to the Author:  
This manuscript describes broad-scale analyses of parental care behaviours in Amphibians. The 
breadth of the study is impressive and represents probably the most extensive data set of parental 
care for this taxon – this is particularly impressive given the wide range of care behaviours found in 
Amphibians. The analyses assess rates and patterns of transitions among care states and categories 
and show that simpler behaviours, such as egg attendance, evolve more rapidly than more complex 
care traits, such as viviparity. The analyses also show that biparental care is likely to be an unstable 
state, with transitions away from biparental care arising at a much higher rate than transitions 
towards biparental care. The manuscript addresses questions of broad interest in a system that is 
particular important for understanding the evolution of parental care. I do have some queries and 
suggestions but I do not anticipate that substantial new analyses are necessary (but see suggestions 
in point 2 and potentially point 4 below).  
 
1) Viviparity as a subdivision of care does not seem well justified. I would argue that it is a life history 
trait that can result in different forms of offspring demands and alters the selection pressures on care 
behaviours, rather than being a care behaviour itself. This distinction might be helpful in terms of 
explaining differences in gains/losses. Perhaps behavioural traits are more labile than life history or 
physiological traits because changes in traits such as viviparity may require more complex 
developmental/genetic changes. Perhaps a more useful/justifiable division would be behavioural 
versus physiological (or anatomical) transitions (see lines 15-18 on page 4).  
 
2) Biparental care is very rare (17 species with complementary care and 14 with overlapping care) 
and I wonder whether this is problematic for the models. It is hard to tell from the figure, but it is not 
clear that any losses are actually observed so it is not clear where the inference of high rates of loss 
comes from and I was left wondering if the result is reliable or whether the model assumptions have 
been violated. With the inferred rate of loss being so much higher than the rate of gain of biparental 
care, it seems remarkable that biparental is observed at all. The challenge of inferring gains and 
losses of binary traits have been discussed and in particular the potential importance of differential 
speciation and extinction has been highlighted (e.g. Goldberg, E.E. and B. Igić. 2008. On phylogenetic 
tests of irreversible evolution. Evolution 62:2727-2741; Goldberg, E.E., J.R. Kohn, R. Lande, K.A. 
Robertson, S.A. Smith, B. Igić. 2010. Species selection maintains self-incompatibility. Science 
330:493-495). Perhaps biparental confers different speciation or extinction rates compared to 
uniparental care and this could explain the distribution of care. It may not be necessary to re-analyse 
the data using such models but at the least some consideration of these alternative mechanisms is 
needed. Although plausible, I don’t think that the results are convincing in terms of stability of 
biparental care, as opposed to care simply being rare. Perhaps a relatively straightforward way to 

assess the reliability of the results would be to simulate a multistate character evolving on the tree 
under the estimated transition rate parameters and assessing the simulated frequency of character 
states compared to the observed – this could be achieved with the sim.character function in the R 
package diversitree. In addition, it would be helpful to see in more detail the distribution of biparental 
care on the tree. These details are in figure 4, panel a but it is hard to read. It either needs to be 
much bigger, or perhaps replotted to show more clearly where overlapping and complementary 
biparental care evolves (i.e. don’t plot the grey circles and instead state that nodes lacking a symbol 
have no biparental care).  
 
3) The raw data do not seem to be available – will they be deposited to e.g. Dryad on publication?  
 
4) Losses in the table in figure 1 don’t seem to be consistent with the transition rates, most obviously 
the rate of loss for tadpole feeding is clearly non-zero in panel c but the number of losses is estimated 
to be zero. The patterns for gains seem consistent (high rate associated with high numbers of gains), 
but losses don’t appear to tally at all. I may have missed something but I wonder if there is an error in 
reporting of these results.  
 
Additional minor comments:  
It would be helpful to report a range or HPDs for transition rates and number of gains losses e.g. page 
8, line 2, and in the supplementary tables (a range would be more helpful than reporting mean, 
median and mode).  
 
Page 3 line 6: “Not only does parental care increase the fitness of offspring and parents”: Is this true? 
If care increases fitness of parent and offspring then there should not be intrafamilial conflict. Isn’t the 
point that care can effect fitness of individuals (offspring, mother, father) differentially and it is this 
variation that cause conflict?  
 
Page 5, lines 10-12: This is a quite hard to follow (what does “parental care forms of diverse 
complexity” mean?).  
 
Methods, page 17, line 14. The description of tree scaling is ambiguous – how was the tree scaled and 
why? Also, why use this rather than the more recent Pyron and Jetz amphibian tree?  
 
Figure 1 - Is grey absence or lack of data? The figure is hard to read because of the small size.  
 
Signed  
Gavin Thomas