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\begin{document}

\title{Refining analyses of existing datasets is valuable for macrogenetics: a
response to Paz-Vinas et al. (2021)}



\author[1]{Katie Millette}%
\author[2]{Vincent Fugère}%
\author[1]{Chloé Debyser}%
\author[3]{Ariel Greiner}%
\author[4]{Frédéric Chain}%
\author[1]{Andrew Gonzalez}%
\affil[1]{McGill University}%
\affil[2]{Université du Québec à Trois-Rivières}%
\affil[3]{University of Toronto}%
\affil[4]{University of Massachusetts at Lowell}%


\vspace{-1em}



  
  \date{June 17, 2024}


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\begin{abstract}
Paz-Vinas et al. (2021) comment on methodological and data-related
limits of our paper (Millette et al. 2020), which affect a small
proportion of our datasets and analyses. These points do not refute our
conclusions. We address their comments and support the call for the
development of best practices for future macrogenetics research.%
\end{abstract}%



\sloppy


\textbf{Title:} Refining analyses of existing datasets is valuable for
macrogenetics: a response to Paz-Vinas et al. (2021)

\textbf{Authors} : Katie L. Millette\textsuperscript{1*}, Vincent
Fug\selectlanguage{ngerman}ère\textsuperscript{2}, Chloé Debyser\textsuperscript{1}, Ariel
Greiner\textsuperscript{3}, Frédéric J. J. Chain\textsuperscript{4} and
Andrew Gonzalez\textsuperscript{1,5}

\textsuperscript{1}McGill University, Department of Biology

\textsuperscript{2}Université du Québec à Trois-Rivières, Département
des Sciences de l'Environnement

\textsuperscript{3}University of Toronto, Department of Ecology \&
Evolution

\textsuperscript{4}University of Massachusetts at Lowell, Department of
Biological Sciences

\textsuperscript{5}Quebec Centre for Biodiversity Science

*\textbf{corresponding author} : Katie L. Millette, Department of
Biology, McGill University, 1205 Docteur Penfield Ave, Montreal QC,
Canada, H4V 2N2

Tel: 514-398-1622; email: millettek@gmail.com

\textbf{Author emails:}

Katie L. Millette: millettek@gmail.com

Vincent Fugère: Vincent.Fugere@uqtr.ca

Chloé Debyser: chloedebyser@gmail.com

Ariel Greiner: ariel.greiner@mail.utoronto.ca

Frédéric J. J. Chain: frederic\_chain@uml.edu

Andrew Gonzalez: andrew.gonzalez@mcgill.ca

\textbf{Statement of authorship:} All authors contributed to the ideas
and writing of the manuscript.

\textbf{Data accessibility statement:} No new data is used.

\textbf{Key words:} macrogenetics, population genetics, intraspecific
genetic diversity, intraspecific genetic variation, COI

\textbf{Type of article:} Technical comment (response to:
ELE-01078-2020.R1 -- Macrogenetic studies must not ignore limitations of
genetic makers and scale)

\textbf{Number of words in abstract:} 52

\textbf{Number of words in main text:} 810

\textbf{Number of references:} 3

\textbf{Number of figures, tables, and text boxes:} 0

\textbf{Abstract}

Paz-Vinas et al. (2021) comment on methodological and data-related
limits of our paper (Millette et al. 2020), which affect a small
proportion of our datasets and analyses. These points do not refute our
conclusions. We address their comments and support the call for the
development of best practices for future macrogenetics research.

\textbf{Main text}

We thank Paz-Vinas et al. for developing aspects of our macrogenetics
paper that we were not able to cover in detail. We agree with some of
their messages and support the call for careful use of compiled data,
particularly when repurposing it for new questions.

Macrogenetics (Blanchet et al. 2017) investigates large-scale patterns
in intraspecific genetic diversity (IGD) across many taxa, as they
relate to ecological processes and anthropogenic impacts. Macrogenetics
is a fast-emerging field, so we hope this exchange with Paz-Vinas
contributes to its development.

Our paper presented a global analysis of the effects of human population
density and land use on patterns of IGD; the first (and most
substantive) part of our paper focused on a spatial analysis and the
second (using a much smaller dataset) presented a time series analysis.
Paz-Vinas et al. comment primarily on the latter.

Paz-Vinas et al.'s comment raises some points we addressed in Millette
et al. (2020) and present two issues that question the main finding of
our paper captured by our title: ``No consistent effects of humans on
animal genetic diversity worldwide''. Yet, nothing in their comment
undermines our conclusions. We address the two major points of their
comment below.

\textbf{Are COI sequences the most appropriate data?}

It is certainly imperfect to use COI sequences for population estimates
of IGD. We gave several reasons in our paper (page 65), including the
inability of mtDNA to reflect neutral evolutionary patterns, and the
potential sensitivity of patterns to the minimum number of sequences per
population (end of page 57).

We are aware of the inconsistent archiving practices among
data-depositors (i.e., uploading only unique sequences to repositories)
and we were careful not to overextend our conclusions because of this.
Paz-Vinas et al.'s recommendation to use haplotype diversity/richness
rather than pairwise nucleotide diversity is valid given the unknown
sampling effort behind archived sequences.

As a community, we must decide whether these limitations preclude the
use of COI in macrogenetics. No other marker offers such broad taxonomic
and spatial scope. Studies using mtDNA reveal large-scale patterns in
IGD with respect to latitude and human impacts (e.g., Miraldo et al.
2016); refining analyses of these existing macrogenetic datasets to
confirm the existence of patterns is necessary to advance the field.
There is an opportunity to gain further insight into IGD patterns by
complementing large-scale analyses with fine-scale population genetic
estimates for data-rich taxa.

\textbf{Are the spatial and temporal scales biologically meaningful?}

Paz-Vinas et al. focus their critique on our time series analyses. Our
analysis does conflate space and time to a certain extent, although we
used the smallest possible spatial scale (1000 km) with sufficient data
to test our hypothesis. We explain this (page 58) and make careful
statements not to over-emphasize these results (i.e., no consistent
effect of humans on animal IGD).

Whether 1000 km exceeds species' dispersal capabilities is
species-specific. Geographic and anthropogenic barriers can further
fragment species' ranges. Because there is no `right' resolution, we
introduced a multi-scale approach to assess IGD patterns at the global
extent. Ideally, species traits, ranges and geological features should
be considered in future studies.

Paz-Vinas et al. selected fish in their comment, which in general have
unique dispersal abilities, and are the most `noisy' taxa in our study
as a result of watershed constraints. We did not account for watershed
structure which is a shortcoming of our analysis, although fish
populations constitute only 11.4\% of our temporal dataset. The purely
spatial analysis, that is the focus of our paper, assesses IGD patterns
at smaller spatial scales (sequences \textless{} 10 km apart) where the
risk of pooling sequences from isolated populations with divergent land
use is reduced. As we have discussed in our Appendix, there is little to
no spatial variation among sequences in the majority of populations:
``\emph{the mean great circle distance among sequences was 0 for
\textasciitilde{}50\% of species in our dataset, and usually \textless{}
100 km for other populations (Fig. S1)} ''. Thus, the ``daisy-chaining''
issue is irrelevant for the majority of our analyses. We would have
liked Paz-Vinas et al. to acknowledge that the issue they raise only
applies to our time series analysis. Future macrogenetic studies should
be aware of the consequences of aggregating sequences into populations.

Regardless of the marker(s) chosen, or method of forming biologically
meaningful populations, Paz-Vinas et al.'s comment does not indicate
either way (positive or negative) how we purportedly over-interpret and
misinform readers on the effects of humans on IGD. Theory predicts
positive and negative effects of humans on IGD, so inconsistent trends
are not surprising.

We agree that macrogenetics will progress faster when researchers align
behind a set of best practices for data, analyses, and the communication
of uncertainties in our understanding of the patterns arising from data
limitations. We look forward to seeing future analyses as the field
tackles the problem of assessing human impacts on genetic diversity.

\textbf{References}

Blanchet, S., Prunier, J.G. \& De Kort, H. (2017). Time to go bigger:
emerging patterns in macrogenetics. \emph{Trends Genet} ., 33, 579--580.

Millette, K.L., Fugère, V., Debyser, C., Greiner, A., Chain, F.J.J. \&
Gonzalez A. (2020). No consistent effects of humans on animal genetic
diversity worldwide. \emph{Ecol. Lett} ., 23, 55--67.

Miraldo, A., Li, S., Borregaard, M.K., Flórez-Rodríguez, A.,
Gopalakrishnan, S., Rizvanovic, M., et al. (2016). An Anthropocene map
of genetic diversity. \emph{Science} , 353, 1532--1535.

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