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\begin{document}

\title{Developing a preprint culture in biology}

\author{Philippe Desjardins-Proulx}
\email[E-mail: ]{philippe.d.proulx@gmail.com}
\affiliation{Theoretical Ecosystem Ecology laboratory, Universit\'e du Qu\'ebec \`a Rimouski, Canada.}
\affiliation{Quebec Center for Biodiversity Science, McGill University, Canada.}

\author{Ethan P. White}
\affiliation{Departement of Bology, Utah State University, United-States of America.}

\author{Joel J. Adamson}
\affiliation{Ecology, Evolution and Organismic Biology, University of North
Carolina at Chapel Hill, United-States of America}

\author{Timoth\'ee Poisot}
\affiliation{Theoretical Ecosystem Ecology laboratory, Universit\'e du Qu\'ebec \`a Rimouski, Canada.}
\affiliation{Quebec Center for Biodiversity Science, McGill University, Canada.}
\affiliation{International Network for Next-Generation Ecology.}

\author{Karthik Ram}
\affiliation{Environmental Science, Policy, and Management. University of California, Berkeley, United-States of America.}

\author{Dominique Gravel}
\affiliation{Theoretical Ecosystem Ecology laboratory, Universit\'e du Qu\'ebec \`a Rimouski, Canada.}
\affiliation{Quebec Center for Biodiversity Science, McGill University, Canada.}

\keywords{Publishing; Preprint servers; Green Open Access; arXiv.}

\maketitle

\section{Introduction}

Public preprint servers allow authors to make manuscripts publicly available
before, or in parallel to, submitting them to journals for traditional
peer-review. The rationale for preprint servers is fundamentally simple: to make
the results of scientific research available to the scientific community as soon
as possible, instead of waiting until the peer-review process is fully completed.
Sharing manuscripts using preprint servers has numerous advantages including: 1) rapid
dissemination of work-in-progress to a wider audience; 2) improved peer review by
encouraging feedback from the entire research community;
and 3) a fair and straightforward way to establish precedence.

Open preprint servers offer a great opportunity for open science, especially if
the community embraces the idea of discussing preprints. Initiatives like
Haldane's Sieve (\href{http://haldanessieve.org/}{http://haldanessieve.org/}), a
new blog discussing arXiv papers in population genetics, will help make arXiv
attractive for scientists looking to promote their work. These initiatives are
important to fully exploit the potential of open preprints servers. Posting
preprints online increases the community of available informal peer reviewers,
and uses the internet for its original community-building purposes.

Preprints began to gain popularity 20 years ago with the advent of arXiv, an open
preprint server widely used in physics and mathematics \cite{gin11}. Preprints
are also integral to the culture of other scientific fields.  Paul Krugman noted
that, in economics, the \emph{traditional model of submit, get refereed,
publish, and then people will read your work broke down a long time ago. In
fact, it had more or less fallen apart by the early 80s} \cite{kru12}. In
addition to a section in arXiv, economists have also the RePEc (Research Papers
in Economics) initiative, which aims to create an archive of working papers,
manuscripts, and book chapters.

Despite the success of this approach in other fields, most manuscripts in
biology are not posted to preprint servers and are therefore not seen by more
than a handful of other scientists prior to publication. In this article, we: 1)
highlight the advantages of open preprint servers for both scientists and
publishers; 2) address several misconceptions about preprints that are common
among biologists; 3) discuss the preprint policies of major publishers in
biology; and 4) review the most popular preprint servers currently available.

\section{The case for public preprints}

The first and most often discussed advantage of arXiv and open preprints is
speed (Figure~\ref{fig:map}). The time between submission and the official
publication of a manuscript can be measured in months, sometime in years. For
all this time, the research is known only to a select few: colleagues, editors,
reviewers. Thus, the science cannot be used, discussed, or reviewed by the wider
scientific community. In a recent blog post, C. Titus Brown noted how posting a
paper on arXiv quickly led to a citation (arXiv papers can be cited) and his
research was used by another researcher \cite{bro12}. The current system of
hiding manuscripts before acceptance pose problems for both scientists and
publishers. Manuscripts that are unknown cannot be used and thus take more time
to be cited. It has been shown that high-energy physics, with its high arXiv
submission rate, had the highest immediacy among physics and mathematics
\cite{pra05}. Immediacy measures how quickly articles are cited. 

Posting manuscripts as preprints also has the potential to result in higher
quality science, by allowing for pre-publication feedback from a large pool of
reviewers. Prepublication reviews by a small network of colleagues are common in
the biological sciences and are an important part of the scientific process.
These "friendly" reviews increases the chances of errors being caught prior to
publication, allow errors to be identified prior to spending months in review,
and allows authors to improve how they communicate the results of their research
by modifying their writing in response to early feedback. Preprint servers offer
a way to extend this network of colleagues to the entire scientific community,
increasing the number of opportunities for review and revision prior to
publication, and resulting in higher quality submissions and publications.  As
such, preprints can be seen as an integral aspect of a vigorous peer-review
process \cite{hoc12}. 

Furthermore, the formal peer-review process as a whole is critically
over-loaded. As the number of active scientists increases and the pressure to
publish increases, it has become increasingly difficult for journals to find
reviewers \cite{hoc09}.  At the same time, rejection rates are high in most
journals \cite{aar08,roh09}, and when not invited to submit a revision, authors
must start the process over again at another journal. As a result, initiatives
to reduce time from submission to publication have emerged across the scientific
community. Rohr et al.  \cite{roh09} called for the recycling and reuse of
peer-reviews: by attaching previous reviews and detailed replies to a new
submission, both the editor and the referees can gauge the work done on the
manuscript, and perhaps evaluate it with less prejudice. In a similar way, the
\emph{Peerage of Science} initiative allows authors to seek anonymous pre-review
by their peers. Some journals now accept to publish papers which received good
evaluations, with \emph{Animal Biology} having recently accepted first a paper
reviewed entirely with the \emph{Peerage of Science} \cite{abb12}, effectively
outsourcing the review process. A widespread use of preprint servers can achieve
the same goal of reducing the time spent in review. By allowing open comments
and criticisms prior to submission, the authors will receive valuable feedback
and can improve the version which will be submitted. With a rich enough
community of scientists depositing preprints, and commenting on them, the
process of an open pre-review can become widespread and will overall increase
the quality of first submissions.

\begin{figure}[ht!] \centering\includegraphics[width=0.50\textwidth]{map.pdf}
\caption { It can take several months, and even a few years, before a submitted
paper is officially published and citable.  The average time to publication
varies greatly between journals and can be as low as 104 days (Evolution for
2011) to 213 (PLOS One in 2010).  Meanwhile, few people are aware of the
research that has been done since, typically, only close colleagues are given
access to the preprints. With public preprint servers, the science is
immediately available and can be openly discussed, analyzed, and integrated into
current research. It benefits both science and publishers. Both want the papers
to be well-known and cited, and public preprints make it possible to integrate
research even before publication, greatly improving immediacy.  }
\label{fig:map} \end{figure}

Finally, public preprint servers offer a fair way to establish intellectual
priority by making the work available when immediately after it is complete.
Some manuscripts will spend much more time in the review process and/or in
production after acceptance, than others. This means that
that publication and acceptance dates do not accurately characterize who
came up with an idea first. For this reason, mathematicians and physicists
have embraced arXiv in part to establish priority in a fair way \cite{gin11,cal12}.

\section{Preprints in biological sciences}

In contrast to other disciplines, the field of biology has effectively no preprint
culture, with the exception of small pockets of primarily highly quantitative
research (e.g., epidemiology). While, submitting to preprint servers has become
more common in the past few years, and the quantitative biology section in arXiv
is experiencing rapid growth in submissions \cite{cal12}, the number of biology
papers submitted to preprint servers still represents only a small fraction of
the total research produced in biology.

There are a number of reasons that biologists have not traditionally had a
culture of sharing preprints, many of which are based on common misconceptions
regarding the costs and benefits of sharing preprints. For example, in contrast
to other fields there is a perception in biology that public preprints
make it easier to steal ideas. However, there is no evidence of this happening
in the numerous other fields that have adopted preprint servers, and since preprint
servers create a clear record of who had the idea first, and when, this
appears to be a largely unfounded concern. In other fields preprints serve the
opposite role, they allow straightforward establishment of precendence, letting
researchs lay claim to an idea thus prevening it from being "stolen".

Another major concern is that if a researcher posts a public preprint that they
will not be allowed to submit their paper to their journal of choice. This is
based on a certain interpretation of the Ingelfinger rule: scientists should not
publish the same manuscript twice \cite{alt96}. However, preprints are not
peer-reviewed papers and posting to a public server does not constitute
publication in a peer-reviewed journal.  A preprint is simply a document that
allows ideas to spread and be discussed, but it is not yet formally validated by
the peer-review system. This is why the majority of publishers do not see arXiv
and similar services as a violation of the Ingelfinger rule. Almost all of the
major publishers in biology are preprint-friendly, including: Nature Publishing
Group, PLOS, BMC, PNAS, Science (mostly) \ref{table:policies}, and all the
journals from Elsevier and Springer.  The Ecological Society of America and the
Genetics Society of America also recently changed their policies to allow public
preprints.  Few scientific publications will not consider a manuscript submitted
to a public preprint server. In fact, \emph{Nature} responded to the rumour that
they refused manuscripts submitted to arXiv by saying that ``\emph{Nature} never
wishes to stand in the way of communication between researchers. We seek rather
to add value for authors and the community at large in our peer review,
selection and editing'' \cite{nat05}. Still, a few journals adopt a ``by
default'' hostile attitude towards preprints, mostly due to the lack of clear
policy of the publishers, or perhaps because a preprint culture has not
developed in biology and the practice is still considered unusual. As an
example, Wiley-Blackwell, which publishes some of the leading journals in
biology, has no official policy on the matter.

\begin{table*}
    \centering
    \begin{tabular}{|ll|}
    \hline
    Publisher                                   & Policy \\
    \hline
    Springer                            	& Accept \\
    BMC                                 	& Accept \\
    Elsevier                            	& Accept \\
    Nature Publishing Group             	& Accept \\
    Public Library of Science           	& Accept \\
    Genetics Society of America                 & Accept \\
    Royal Society                       	& Accept \\
    National Academy of Science (USA)           & Accept \\
    Ecological Society of America       	& Accept \\
    Oxford Journals                             & Accept \\
    Science                             	& Ambiguous \\
    Wiley-Blackwell                       	& No general policy \\
    British Ecological Society                  & No answer to our query \\
    \hline
    \end{tabular}
    \caption{Policies for important publishers in biology. Some publishers
tolerate preprints except for a few of their medical journals, e.g.: Journal
of the National Cancer Institute from Oxford and The Lancer from Elsevier.}
    \label{table:policies}
\end{table*}

\section{Current offerings}

We briefly discuss the main options to submit preprints to open servers:
arXiv.org, figshare, and the upcoming PeerJ and F1000Research.

\subsection{arXiv}

arXiv (\url{http://arxiv.org/}) is the most widely-used preprint server today,
and its use is almost universal in some branches of mathematics and physics.
arXiv provides a reliable citation system for all eprints and is especially
popular in high-energy physics. Physicist Paul Ginsparg created arXiv in 1991
for theoretical high-energy physicists to communicate preprints via email and
ftp, and soon thereafter adopted the newly created world-wide
web\cite{jackson2002preprints}.  arXiv now receives over 7 000 submissions per
month (\url{http://arxiv.org/show_monthly_submissions}) and divides its
submissions into subcategories of physics, mathematics, computer science,
quantitative biology, finance and statistics.  The quantitative biology category
includes subcategories for Populations and Evolution, Quantitative Methods and
other categories that may be of interest to biologists.

One aspect of arXiv that differs from other options is that it has a moderation
system, which requires that papers must be categorized by an endorser.
At least one author of a paper must be an endorser that has previously submitted
a paper or has received permission to submit to a particular category. arXiv is now
administered by the Cornell University Libraries, with funding coming from
voluntary pledges by academic institutions along with matching funds from the
Simons Foundation \cite{arxiv_future}. This approach to financing is one of
the numerous measures that arXiv takes to ensure that the repository will remain
permanently available and submissions will be readable.

\subsection{figshare}

figshare (\href{http://figshare.com}{http://figshare.com}) is an open server
that allows scientists to submit any research output: manuscript, figures,
datasets, videos, theses, presentations, and so on. There are no rules to limit
what constitutes a research output and, unlike arXiv, there is no endorser
system. All figshare content has a unique digital object identifier (DOI) like
any journal article, thus offering a permanent and stable link to the content.
A flexible tag system is used to classify each item. Comments can be made on all
content allowing for centralized discussion related to the material.

One of the advantages of figshare over arXiv for biologists is that is it not limited
to quantitative sciences. arXiv.org has sections on quantitative biology but might
not be appropriate for non-quantitative work. With its flexible approach to
preprints, figshare offers an alternative to arXiv for empirical
biologists. Furthermore, by allowing all types of content, figshare also
provides an archive for early results (e.g.: figures, lab presentations).

\subsection{PeerJ}

PeerJ (\href{https://peerj.com/}{https://peerj.com/}) is a new Open Access
publisher that combines both a preprint server, and a peer reviewed journal.
It is focused on the biological and medical sciences, which may help overcome the
perception that preprints do not have a place in biology. Like figshare this is
an advantage relative to arXiv for biologists doing non-quantitative work.
Also like figshare PeerJ allows commenting on posted preprints, improving the
potential for pre-publication
dialog. In addition, preprints can be made private if the authors choose, and
shared only with selected colleagues. While this reduces many of the benefits of
preprints described above, it may allow some researchers who would not otherwise
post preprints to begin to explore the possibility in a manner appropriate to
their current circumstances.

In contrast to other preprint servers users cannot post unlimited public
preprints for free. One preprint per year can be posted for free, with a onetime
(i.e. lifetime) fee of 99 dollars required to allow an author to post unlimited public
preprints. The preprint server is not tied to the journal, so preprints can be posted
regardless of where they will eventually be submitted for publication.

\subsection{F1000Research}

F1000Research is not a public preprint server like the previous three servers.
Whereas arXiv, figshare, and PeerJ offer an option to submit a manuscript
without having it reviewed, papers submitted to F1000Research will eventually be
reviewed. Thus, F1000Research offers a hybrid model with publicly available
manuscripts at time of submission and standard peer-reviews that occur as part
of the submission process. Manuscripts are
considered ``accepted'' and will only be indexed after two positive referee
responses. F1000Research works closely with data providers to integrate raw
data to the paper. For instance, upon submitting a paper, authors are asked to
upload their data, which are then integrated in \emph{e.g.} figshare widgets,
the DOI of which are given in the paper when the data are first mentionned.
By integrating data to the paper, F1000Research is working to make
science more reproducible and open.

\subsection{GitHub}

This manuscript was developed entirely as an open project on GitHub. GitHub is
one of several hosting services for collaborative development using the Git
version control system (VCS).  Git is a decentralized revision control system
created by Linus Torvalds and is used primarily to develop software, including
the Linux kernel. Git provides powerful features that allow numerous
contributers to work asynchronously on the same project, often in parallel
branches, all of which can be effortlessly merged and version controlled.  While
Git is created primarily for software development, where the use of version
control systems is standard \cite{aru12}, it is ideal for academic research
since it provides a way to collaborate on every step of the manuscript
development process, from data manipulation and analysis to writing and
revision. For example, during the development of this manuscript, each author
would clone the project (\emph{i.e.} make a personal copy), modify it, and then
merge their changes into a master branch. This takes the preprint process to an
entirely new level, where the entire writing process is open from the beginning.

\section{Conclusion}

The ongoing discussions on the publication process, peer-reviewing and
alternative publication models are all symptoms of the current uneasiness of
scientists with the ever growing obsession with bibliographic metrics such as
the impact factor \cite{Fisher2012}. There is pressure on researchers, wether
they are junior looking for an academic position or senior trying to secure
funding for their team, to orient their publication strategy in order to
maximize their number of publications and total citations. A well-known
consequence is to submit manuscripts first to the most prestigious journals, and
then resubmit to lower level journals as they are rejected. The numerous
negative impacts of such behavior have been discussed in depth \cite{hoc09} and
include a long delay between the time a manuscript is finished to its
publication.  They all contribute somehow in a general slowing down of
scientific progress.  Research activities and the publication process are
drifting away from their fundamental object, namely the diffusion of novel
scientific discoveries. 

Developing a preprint culture in biology is not a final solution to the impact
factor inflation, it might however reduce significantly its negative
consequences. Preprints speed up publication, openly, with no judgement on
pertinence and originality. Paradoxically, because peer-reviewing is conducted
following this step in the process of a scientific communication, it might bring
it closer to its fundamental objective. The role of peer-reviewing is to judge
the scientific quality of a study, the match between its hypotheses, methods,
results and conclusions. The peer review process is the first barrier against
fraudulent or bad quality science, susceptible to impede scientific progress. It
is however now dominated by subjective evaluations, where trendy contributions
are promoted to increase the immediacy impact of the journal. Most journals have
in their instructions for reviewers a section devoted to the evaluation of
suitability for the journal, a task usually incumbent to editors. Preprints are
by definition not evaluated, neither for their quality nor their pertinence.
Technically, the difference between a preprint and a traditional publication
should be that the latter as the approval stamp by pairs on its quality. The
relevance of a study, its contribution to science, should only be judged
post-publication by many more readers than the typical two-four anonymous
reviewers. With a such a shift in the diffusion strategy, the role of
traditional journals and their editors would be to showcase scientific
discoveries for specialized readership. Such a process should improve even
further their diffusion, not impede it. 

The current opening of the publication process we are currently witnessing with
the arrival of new preprint systems and innovative publication models such as
F1000, PLOS One, Nature Scientific Reports, might significantly bypass the
inflation of bibliographic metrics. They not only promote scientific communications
by changing the focus of peer-reviewing, they also favor the publication of
results that might otherwise be rejected because of low interest, negative
results, descriptive and quantitative studies and datasets. One of drawback of
making publication easier is obviously the proliferation of studies of uneven
quality. A tradeoff between the intensity of the peer-review filtering and the
benefits to science has been hypothesized \cite{Aarssen2012}. With increasingly
stringent peer reviewing, the quality of published papers and easiness of
finding discoveries might increase, at the cost of censorship, increasing load
on authors and reviewers and time for publication. Preprints are simply
bypassing this model, for what we believe is the progress of science: they speed
up the dissemination of scientific discoveries, impede censorship and put on
reader's shoulders the responsibility to judge originality and pertinence.

\section{Funding}

PDP is supported by an Alexander Graham Bell scholarship from the National
Sciences and Engineering Council of Canada. EPW is supported by a CAREER Award
from the National Science Foundation (DEB-0953694). JJA is supported by NSF
DEB-0614166 and NSF DEB-0919018.  TP is supported by a FQRNT-MELS post-doctoral
scholarship and 25 cents found by a coffee machine.  KR is supported by NSF
DEB-1021553. DG is funded by a Discovery Grand from the National Sciences and
Engineering Council of Canada and by the Canada Research Chair program.

\section{Acknowledgements}

We thank Carl Boettiger and Mark Hahnel for helpful comments on an earlier
version of this manuscript.

\newpage
\bibliography{refs}

\end{document}