Quantitative genetics for a more qualitative conservation

Mainly satisfied with the modifications to the manuscript which have fulfilled my previous comments. Argumentation is now clearer and more precise. The only point where I have still some concerns is related to the ambiguity regarding the citation of the classical management methodology currently being applied in ex-situ conservation programs. In several places of the manuscript (e.g., line 65 or line 399) the expression ‘mate-pairing based on kinships’ seems to mean that minimisation of the kinship (coancestry) is only used to decide the mating scheme to limit the rise of inbreeding when, actually, this parameter is also to be accounted in the selection process itself, determining the ‘redundant’ individuals or the ones belonging to underrepresented lineages which should be promoted to produce offspring (maintenance of the genetic diversity). 

Additionally, I detected a couple of typos:

-          Line 91: ‘ … integration OF quantitative …’

-          Line 177: Something missing between ‘variance’ and ‘different’. Suggestion: ‘ … is due to …’ or something similar.

This is the second time I review this manuscript. I think the authors edited the manuscript appropriately in response to the first round of reviews and I do not have any more comments. I think this manuscript should now be recommended and that it will be a very useful addition to the litterature on ex-situ conservation (and also a nice review of quantitative genetic methods for wildlife more in general).

Improving species conservation plans under IUCN’s One Plan Approach using quantitative genetic methods, by Sauve and coworkers. The authors review the aspects that have to be taken into account when managing exsitu conservation programs regarding the coordination with the wild populations. They also comment on the methods (especially quantitative genetics) available to be implemented. I find this study very useful to rise the concern on the stakeholders that conservation cannot be split into insitu and exsitu actions but have to deal with the population as a whole and coordinate aims and methods with the final goal of guaranteeing stable and far-from-risk populations in the wild (the known as One Plan Approach). In this regard, I think this is a timely and needed exercise.

Simplifying a bit, or being pragmatic, the required change of paradigm in the management of (exitu) conservation populations is to go beyond the classical idea of maintaining general (neutral) genetic diversity and including adaptive variation into the goals and criteria. Obviously, if we maintain plenty of general genetic variation, hopefully also adaptive variation will remain (drift affects the whole genome). However, if there is information on genetic conformation for fitness-related traits the probability of survival of the population will be higher by including it into the management procedures. The new philosophy would be performing some kind of ‘selection’ for key traits while maintaining general genetic diversity. This is the objective of the Optimal Contribution (OC) theory (Meuwissen 1997, J. Anim. Sci. and posterior developments) that it is common in breeding programs of commercial populations. This OC could be mentioned in the paper to widen the methodological options for managers. Actually, fitness is already accounted for in the management of conservation programs when (mono)genetic defects appear by avoiding the use of carriers of the deleterious allele. The new situation implies dealing with more or less infinitesimal traits and, thus, the need of applying quantitative genetics methods.

A large amount of the submitted text is devoted to the relevant problem of plasticity. However, I think that in the manuscript plasticity is mixed and somehow confounded with GxE interaction. The latter is related with adaptation to captivity (even if both environments are stable) as the relative performance between genotypes may be different in captivity and the wild and, in the extreme, the best fitted genotype exsitu has a poor performance in the wild. GxE interaction can be dealt with more easily by performing multitrait evaluations (phenotype in captivity and nature considered different traits). Then captive individuals can be evaluated for their expected performance in the wild and used as parents of the next generation (or not). No need to measure the same individual in captivity and the wild but having relatives in both environments. For example, a parent can be evaluated by their released offspring.

Contrarily, detecting the effects of captivity on the plasticity of individuals would imply a greater sampling/recording effort. The feasibility of the use of plasticity as a criterion should be critically included in the manuscript. For example: how to determine the key traits for adaptation/plasticity in the wild? What are the required sampling sizes to obtain enough accuracies? In the end, everything is related to the importance of planning the captivity environment to minimise the differences with the wild (and to what extent this is possible).

Anyway, in the absence of further information, aiming at neutral variation minimises drift, the changes in allelic frequencies and the adaptation to captivity. Thus, it is not as bad as implicit in some of the comments in the text.

The study would benefit from the inclusion of a (brief) discussion on the extra advantages that molecular information could provide to the One Plan Approach management. For example (but not limited): i) determining founder relationships in exsitu populations; ii) trace lineages from released individuals (descendants of reintroduced); iii) detect genomic regions involved in adaptation (differences between wild and captive populations).

I would also want to point out to a problem on the format of the manuscript. Throughout the manuscript plenty of redundancies can be found, with the same idea presented several times. This enlarge (unnecessary) the text and makes the reading more tiring. 

Further comments follow:

- Lines 44-45: I would include in the list those captive populations created in specific centres (i.e. for single species) not fitting the traditional definition of zoos. I think that such populations offer more opportunities for the management and more powerful actions can be conducted.

- Line 51: I think you should be more precise with the expression ‘the potential for reduced reproductive fitness’ when listing the challenges in the management of ex situ populations by highlighting that you mean the failure to reproduce in the wild once released (adaptation to captivity). Because, in general, ex situ populations perform reproductively well, mainly due to the benign environment. Moreover, as the next part of the sentence says ‘adaptation to captivity’ it may lead to think that they are different factors. If you mean loss of fitness due to inbreeding depression, I think that the problem of inbreeding is usually worse in the wild than in (well) managed ex situ populations.

- Line 65: This citation is missing in the References section.

- Line 70: The concept of ‘realities’ could be a bit expanded commenting on the conflict optimal vs. feasible as well as the problem of the expected vs. the observed outcomes. The latter sometimes arises because of some factors not accounted leading to evolutionary changes (line 72) due to unintentional selection (line 74).

- Lines 75-76: This is what I expressed in my general comments. Not only neutral unspecific diversity should be preserved by minimising coancestry, but also data on adaptive diversity should be included in the management criteria.

- Line 94: There is no Section 6. There is a mismatch between number of sections and the description of the contents.

- Line 156: The average breeding value is a parameter of a trait, not of a phenotype.

- Line 164: Avoiding evolutionary change can be pursued by controlling the breeding values for specific traits or, in a general way, by minimising the changes in the genetic makeup due to drift. Saura et al. (Cons. Genet. 2008) already proved that minimising coancestry (even from pedigree information) lead to the smallest change in allelic frequencies. More recently, different authors (Meuwissen et al. 2000, Front. Genet., Morales-González et al. 2021, Genes) explored the effects on the change of allelic frequencies from the use of different molecular coancestry matrices in the management of conservation programs.

- Lines 182-183: This sentence is a bit misleading due to the expression ‘contribute’. I think that something like ‘affect’ or ‘has a great influence in the performance for important traits’. Moreover, this is also true for large populations, at least for the part of the genetic variation.

- Lines 195-196: I find this sentence a bit ‘speculative’ because in practical terms new captures to be included in ex situ populations are mainly opportunistic. It is quite difficult to pick up the individual with the required neutral variation to enlarge the genetic background of the population and it may be even harder to detect the one with the ‘appropriate’ breeding value.

- Lines 208-209: Please, rewrite the definition of Animal Model; it seems that all individuals have to be founders with not known ancestors to apply this methodology. Additionally, there are developments of Animal Model methodology that allows for the several populations, for example in crossbreeding selection schemes where not only (additive) breeding values can be estimated but also dominant effects calculated and accounted for.

- Line 212 and followings: And alternative for the genetic groups is the use of molecular information in a punctual way to estimate the genetic relationships between founders or to apply the concept of ‘metafounders’ in the evaluation of the genetic merit.

- Lines 218-219: The original idea of the concept of ‘genetic groups’ was to account for the fact that different founders might come from different populations (with different genetic backgrounds). For example when a single captive population is constructed by sampling individuals from several isolated regions. If new captures occurs in the same original population a not much different background is expected (in general) as to consider that is a different genetic group. Moreover, when is time to change to a new group? Two generations? Five?

- Lines 220-221: This feature is not (completely) related to the definition or not of genetic groups. Even if all founders are assumed to be from the same group, the proportion of insitu (founders’ contribution) and exsitu (non-founders’ contribution) influence in the genome can be calculated from the pedigree and monitored.

- Line 265: Replace ‘a’ by a comma.

- Line 265: From this moment it seems that all references to figures are wrong. Here it should be Fig. 4 instead Fig. 3, shouldn’t it?

- Line 292: As said before, I find quite difficult to detect plasticity but detect differences in genetic conformation by evaluating the differences in phenotype (Animal Model).

- Line 299: There is a missing ‘of’ between ‘impacts’ and ‘captivity’.

- Line 308: I agree with the authors that differences in social interactions between exsitu and insitu populations are crucial to determine the success of reintroductions. At the same time I think it is the most difficult aspect to be accounted for when ‘naturalising’ the  captive environment.

- Line 318: In most captive breeding programs hand-reared animals are never used for reintroductions.

- Line 320: The correct spelling is Callithrix (missing ‘i’).

- Lines 335-336: Not very informative on what you will find in this section. It is plenty of lines on software.

- Line 339: Missing ‘in’ between ‘maintained’ and ‘a variety’.

- Lines 342-343: Rewrite to avoid the use of ‘options’ twice.

- Lines 350-351: It must be highlighted that (Estimated) Breeding Values are dynamic values and should be updated in the database every time a new evaluation is performed. It is not like phenotypic value for a trait (e.g. size at birth) that doesn’t change even if the individual grows up and is bigger at another age.

- Lines 357-360: I think that one of the main messages of the paper should be that different sources of information and different goals have to be included into the management criteria beyond the maintenance of global genetic diversity (minimisation of coancestry).

- Line 361: To be consistent with the part about the studbook and population management, some examples of QG software could be provided (for example programs to perform breeding values estimation).

- Lines 363-364: This sentence is incomplete.

- Line 367: It is not only the need of accuracy (e.g. pedigree completedness) but also to a standardisation of the way the measurements are taken between different facilities and across generations.

- Lines 372-373: This is the hard task. It would be nice to have a deeper consideration on the real applicability of these methodologies and to provide examples of cases where the situation is closer to this scenario and those where it would be nearly impossible.

- Lines 385-386: I think that the main task conducted in current exsitu conservation programs is the priorisation of individuals to be reproduced based on their genetic relationship with the rest (before/besides the minimisation of the coancestry between pairs). This procedure acts jointly on the maintenance of genetic diversity and the minimisation of the rise of inbreeding.

- Line 402: I agree. It is clear that studies on insitu populations are needed to know the target traits and values to be pursued in captivity. And the same goals should be established for both environments.

- Line 404: It is difficult to deal with fitness itself. Sometimes it is more useful to concentrate on particular traits (main components of fitness).

- Line 405: There is an extra space before Bonnet.

- Line 409: Something missing between ‘be’ and ‘to’.

- Line 418: I think that the first/main aim is to reduce the loss of diversity. Minimising inbreeding is a complementary aim, which should go together. Realise that it is hard to minimise inbreeding when little genetic diversity is present.

- Line 664: Capitalise Fisher and Wright.

- Line 696: Provide a caption to the Figure 2. Additionally, I think that the information presented in the left and right parts of the figure are different enough to deserve separated figures.

- Line 698: Is the word ‘in’ really needed between ‘individuals’ and ‘might’?

- Line 700: Change the word ‘or’ by ‘and’ because in this scenario differences in environment.