Seasonally migratory songbirds have different historic population size characteristics than resident relatives

Reviewer #1 (Public Review):

Summary:
This interesting study applies the PSMC model to a set of new genome sequences for migratory and nonmigratory thrushes and seeks to describe differences in the population size history among these groups. The authors create a set of summary statistics describing the PSMC traces - mean and standard deviation of Ne, plus a set of metrics describing the shape of the oldest Ne peak - and use these to compare across migratory and resident species (taking single samples sequenced here as representative of the species). The analyses are framed as supporting or refuting aspects of a biogeographic model describing colonization dynamics from tropical to temperate North and South America.

Strengths:
At a technical level, the sequencing and analysis up through PSMC looks good and the paper is engaging and interesting to read as an introduction to some verbal biogeographic models of avian evolution in the Pleistocene. The core findings - higher and more variable Ne in migratory species - seem robust, and the biogeographic explanation is plausible.

Weaknesses:
I did not find the analyses particularly persuasive in linking specific aspects of clade-level PSMC patterns causally to evolutionary driving forces. To their credit, the authors have anticipated my main criticism in the discussion. This is that variation in population size inferred by methods like PSMC is in "effective" terms, and the link between effective and census population size is a morass of bias introduced by population structure and selection so robustly connecting specific aspects of PSMC traces to causal evolutionary forces is somewhere between extremely difficult and impossible.

Population structure is the most obvious force that can generate large Ne changes mimicking the census-size-focused patterns the authors discuss. The authors argue in the discussion that since they focus on relatively deep time (>50kya at least, with most analyses focusing on the 5mya - 500kya range) population structure is "likely to become less important", and the resident species are usually more structured today (true) which might bias the findings against the observed higher Ne in migrants.

But is structure really unimportant in driving PSMC results at these specific timescales? There is no numerical analysis presented to support the claim in this paper. The biogeographic model of increased temperate-latitude land area supporting higher populations could yield high Ne via high census size, but shifts in population structure (for example, from one large panmictic population to a series of isolated refugial populations as a result of glaciation-linked climate changes) could plausibly create elevated and more variable Ne. Is it more land area and ecological release leading to a bigger and faster initial Ne bump, or is it changes in population connectivity over time at expanding range edges, or is the whole single-bump PSMC trace an artifact of the dataset size, or what? The authors have convinced me that the Ne history of migratory thrushes is on average very different from nonmigrant thrushes, but beyond that it's unclear what exactly we've learned here about the underlying process.

I generally agree with the authors that "at present there is no way to fully disentangle the effects of population structure and geographic space on our results". But given that, I think there are two options - either we can fully acknowledge that oversimplified demographic models like PSMC cannot be interpreted as supporting evidence of any particular mechanistic or biogeographic hypothesis and stop trying to use them to do that, or we have to do our best to understand specifically which models can be distinguished by the analyses we're employing.

Short of developing some novel theory deep in the PSMC model, I think readers would need to see simulations showing that the analyses employed in this paper are capable of supporting or refuting their biogeographic hypothesis before viewing them as strongly supporting a specific biogeographic model. Tools like msprime and stdpopsim can be used to simulate genome-scale data with fairly complex biogeographic models. Running simulations of a thrush-like population under different biogeographic scenarios and then using PSMC to differentiate those patterns would be a more convincing argument for the biogeographic aspects of this paper. The other benefit of this approach would be to nail down a specific quantitative version of the taxon cycles model referenced in the abstract, and it would allow the authors to better study and explain the motivation behind the specific summary statistics they develop for PSMC posthoc analysis.

Reviewer #2 (Public Review):

Summary:
Winker and Delmore present a study on the demographic consequences of migratory versus resident behavior by contrasting the evolutionary history of lineages within the same songbird group (thrushes of the genus Catharus).

Strengths:
I appreciate the test-of-hypothesis design of the study and the explicit formulation of three main expectations to test. The data analysis has been done with appropriate available tools.

Weaknesses:
The current version of the paper, with the case study chosen, the results, and the relative discussion, is not satisfying enough to support or reject the hypotheses here considered.

The authors hypothesized that the wider realized breeding and ecological range characterising migrants versus resident lineages could be a major drive for increased effective population size and population expansion in migrants versus residents. I understand that this pattern (wider range in migrants) is a common characteristic across bird lineages and that it is viewed as a result of adapting to migration. A problem that I see in their dataset is that the breeding grounds range of the two groups are located in very different geographic areas (mainly South versus North America). The authors could have expanded their dataset to include species whose breeding grounds are from the two areas, regardless of their migratory behaviour, as a comparison to disentangle whether ecological differences of these two areas can affect the population sizes or growth rates.

As I understand from previous literature, the time-scale to population growth and estimates of effective population sizes considered in the present paper for the resident versus migratory clades seem to widely predate the times to speciation for the same lineages, which were reported in previous work of the same authors (Everson et al 2019) and others (Termignoni-Garcia et al 2022). This piece of information makes the calculation of species-specific population size changes difficult to interpret in the light of lineages' comparison. It is unclear what the authors consider to be lineage-specific in these estimates, as the clades were likely undergoing substantial admixture during the time predating full isolation.

Regarding the methodological difficulties in interpreting the impact of population structure on the estimates of effective population sizes with the PSMC approach, I would think that performing simulations to compare different scenarios of different degrees of structured populations would have helped substantially understand some of the outcomes.

Additionally, I have struggled to understand if migratory behaviour in birds is considered to be acquired to relieve species competition, or as a consequence of expanded range (i.e., birds expand their range but their feeding ground is kept where speciation occurred as to exploit a ground with higher quality and abundance of seasonal local resources).

The points raised above could be considered to improve the current version of the paper.

Reviewer #3 (Public Review):

Summary:
This paper applies PSMC and genomic data to test interesting questions about how life history changes impact long-term population sizes.

Strengths:
This is a creative use of PSMC to test explicit a priori hypotheses about season migration and Ne. The PSMC analyses seem well done and the authors acknowledge much of the complexity of interpretation in the discussion.

Weaknesses:
The authors use an average generation time for all taxa, but the citations imply generation time is known for at least some of them. Are there differences in generation time associated with migration? I am not a bird biologist, but quick googling suggests maybe this is the case (https://doi.org/10.1111/1365-2656.13983). I think it important the authors address this, as differences in generation time I believe should affect estimates of Ne and growth.

The writing could be improved, both in the introduction for readers not familiar with the system and in the clarity and focus of the discussion.