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Advancing Equity and Inclusion in Microbiome Research and Training



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Advancing Equity and Inclusion in Microbiome Research and
Alicia J. Foxx,
Karla P. Franco Meléndez,
Janani Hariharan,
Ariangela J. Kozik,
Cassandra J. Wattenburger,
Filipa Godoy-Vitorino,
Adam R. Rivers
U.S. Department of Agriculture, Agricultural Research Service, Gainesville, Florida, USA
Cornell University, Ithaca, New York, USA
University of Michigan, Ann Arbor, Michigan, USA
University of Puerto Rico, School of Medicine, San Juan, Puerto Rico, USA
Karla P. Franco Meléndez, Janani Hariharan, Ariangela J. Kozik and Cassandra J. Wattenburger contributed equally to this work.
ABSTRACT This article proposes ways to improve inclusion and training in microbiome
science and advocates for resource expansion to improve scientic capacity across insti-
tutions and countries. Specically, we urge mentors, collaborators, and decision-makers
to commit to inclusive and accessible research and training that improves the quality of
microbiome science and begins to rectify long-standing inequities imposed by wealth
disparities and racism that stall scienticprogress.
KEYWORDS collaboration, equity, inclusion, international, mentoring, microbiome,
Microbiome research is being applied to important global challenges like pan-
demic preparedness, infectious disease prevention, climate change, and food se-
curity. This research is currently concentrated in a few resource-rich countries (1) which
limits the eld in several ways. The best solutions to these global challenges come
from the work of scientists who understand the cultural and logistical needs of imple-
menting solutions in their communities. The microbiomes of natural, host-associated,
and built environments vary geographically, so undersampling large regions of the world
limits our understanding of microbial communities (2, 3). This leaves a valuable subset of
the microbial biosphere uncharacterized and a valuable subset of researchers excluded.
Changes to microbiome science that increase scientic opportunities for persons histori-
cally excluded due to ethnicity and people from low- and middle-income countries will
improve the quality of research in the eld as well as being the right thing to do.
Persons who identify as Black or African American, Latinx or Hispanic, and peoples
indigenous to land comprising the United States and its territories (henceforth called
PEERs for persons excluded due to ethnicity or race) (4, 5) have been excluded from,
and therefore underrepresented in microbial science, and the sciences more broadly.
Scientists from low- and middle-income countries (LMICs) are similarly underrepre-
sented in contemporary science. To make microbiome science global, equitable, and
inclusive, and thus serve everyone, we explicitly focus on support for PEER and LMIC
scientists and trainees. These groups differ in the challenges they face for different
socio-political reasons, but we identify common needs and advocate for changes and
resources aimed at improving inclusion and access to microbiome research. This article
Citation Foxx AJ, Franco Melendez KP,
Hariharan J, Kozik AJ, Wattenburger CJ, Godoy-
Vitorino F, Rivers AR. 2021. Advancing equity
and inclusion in microbiome research and
training. mSystems 6:e01151-21. https://doi
Editor Benjamin E. Wolfe, Tufts University
This is a work of the U.S. Government and is
not subject to copyright protection in the
United States. Foreign copyrights may apply.
Address correspondence to Alicia J. Foxx,, or Adam R. Rivers,
This piece proposes ways to improve
inclusion and training in microbiome science
and urges decision-makers to commit to
rectifying long-standing inequities imposed by
wealth disparities and racism that stall scientic
Published 12 October 2021
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is intended to start a conversation within the microbiome community, and we provide
resources for persons in decision-making positions (e.g., principal investigators, men-
tors, collaborators, funders, administrators, professional societies) to implement and
invest in equity in science and health (Fig. 1).
PEER scientists. The systematic exclusion of PEERs from academic and scientic
pursuits contributes to the persistent underrepresentation of PEER individuals in the
microbial sciences (4, 6). Decades of efforts have failed to lead to major, sustained
increases in representation of PEER scientists, especially in leadership roles and other
positions of inuence; this is especially acute in microbiology (7). Recent critiques have
highlighted the need to shift narratives (and therefore solutions) away from a decit
framework and toward making changes to institutions themselves. A decit framework
focuses only on diversity and emphasizes a perceived lack of ability or tof PEER indi-
viduals. However, improvements can be made by prioritizing the transformation of teach-
ing, training, and research environments to better serve PEER individuals and an organiza-
tion as a whole (8). This transformation requires a commitment to equity and inclusion
that includes stakeholders at all levels and a willingness to identify and address structural
and systemic barriers (9). Challenges exist at every step from recruitment into undergradu-
ate and graduate training through promotion and tenure (1012), mentoring (13, 14),
FIG 1 Decision-makers, key areas of change within the microbiome sciences, and actions that will foster
inclusion for PEER and LMIC scientists in microbiome sciences.
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appointment to leadership positions (7, 15), career development for nonacademic pursuits
(16, 17), publishing (1821), and acquisition of funding (2225). However, PEERs in the mi-
crobial sciences are expected to persist despite cultures that devalue them and their tal-
ents. The institutions that have historically served PEER scientists like American community
colleges, tribal colleges, and historically black colleges and universities often contend with
reduced access to resources and infrastructure needed to train students in computing and
communication skills (2628). There is a need for bold, resourced, and strategic programs
that support the careers and training of PEERs in microbiome sciences, their matriculation
to leadership positions, and the transformation of programs, departments, and organiza-
LMIC scientists. Like PEER scientists, LMIC scientists bring a wealth of talent, ideas,
and perspectives that would enrich the scientic process and culture, and yet, researchers
from both groups often lack opportunities to acquire the training, funds, and support to
make signicant contributions to their elds. Countries holding economic and technologi-
cal wealth must cooperate synergistically with LMICs to promote their participation and
leadership in research for a more globally inclusive microbiome training agenda (2932).
In Table 1, the Guidelines for equitable collaboration and mentoring practices with LMIC
and PEER scientistsdetail resources that have been successfully used toward developing
guidelines that promote equitable research collaborations between well-funded research
TABLE 1 Organizational resources and examples of equitable research and mentoring practices with LMIC and PEER scientists and trainees
Theme Resources
Guidelines for equitable collaboration and
mentoring practices with LMIC and PEER scientists
Montreal Statement on Research Integrity in Cross-Boundary Research Collaborations (33):
guidance on agreements and responsibilities when engaging in cross-national, -institutional,
and -disciplinary research
The Swiss Commission for Research Partnership with Developing Countries (34) and The
Research Fairness Initiative (35, 36): organization and program for equitable collaboration
with LMIC scientists
The Nagoya Protocol (37): equitable access and benet-sharing of genetic resources
National Academy of Sciences, Engineering, and Medicine mentoring report (38): guidance on
inclusive mentoring practices
IDEA Network of Biomedical Research Excellence (INBRE): support for research, mentoring,
collaboration. and faculty training in Puerto Rico (
Microbiome-focused equitable partnerships The Earth Microbiome Project (39): a global initiative focused on the development of standard
operating procedures for the characterization of the earth microbiome
The international Human Microbiome Standards ( a
global initiative focused on the development of standard operating procedures for the
characterization of the human microbiome
The Benioff Center for Microbiome Medicine (
-diversity-equity-and-inclusion): example of PEER support and in microbiome sciences
Team building and communication resources Cold Spring Harbor Laboratory Leadership in Bioscience Workshop (
courses.aspx?course=c-leader&year=19): workshop on effective leadership and mentoring in
EMBO Laboratory Leadership course ( leadership courses
with an emphasis on research and research dissemination
Springer Nature Effective Collaboration course (
-effective-collaboration-in-research/17078834): course on effective collaboration in science
UCSF The Scientic Leadership and Management Skills course (
example of a leadership program for postdoctoral researchers in sciences
Microbiome training and conference-based support
for LMIC and PEER scientists
International Society for Microbial Ecology (
Ambassador program with global organizations for workshops and activities
The Microbiota Vault ( and MV-Global Microbiome Network
(GloMiNe) symposia: example of global symposium with the goal of education to promote
preservation of microbial ecosystems in nature and in collections
Codes of ethics at conferences to support underrepresented scientists (40)
Guidelines for organizing an intentional bioinformatics training in LMIC (41)
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institutions and LMIC scientists. When establishing global partnerships for microbiome
research, consider following the guidelines and successful examples detailed in Table 1.
Existing international programs in microbiome surveying (Table 1, Microbiome-focused
equitable partnerships) show that equitable partnerships in this eld are not only possible
but are successful through sharing of resources, project responsibilities, and funding. Their
contributions to the eld include signicant microbiome curation efforts, including the
design of standard protocols for sample collection and processing, data analysis, and data
sharing (39). We propose that these and other international working groups, already at the
forefront of microbiome research, serve as exemplars in the creation of guidelines for in-
clusive and equitable collaborations with LMIC scientists.
We also highlight more specic pathways toward training and research practices
that enrich the experiences of both LMIC and PEER scientists that scientists from high-
income countries (HIC) can take up. For mentoring and collaboration, HIC scientists
can create mentoring communities with more than one mentor to provide various per-
spectives for PEER and LMIC mentees (38) and understand and dismantle power dy-
namics associated with privilege within PEER mentorship. Mentors and collaborators
from positions of privilege should counteract factors that negatively affect menteesexpe-
riences (e.g., combating institutional racism) and should employ culturally responsive men-
toring and collaboration which embraces questions asked by PEER and LMIC scientists
that are important to their cultural identities but may differ from norms set by Western or
white scientists (38, 4246). These scientists should engage in mentor and collaborator
training such as team-building courses to communicate roles and responsibilities effectively
and improve team productivity (Table 1, Team building and communication resources)
and should model expectations for an inclusive environment and practice transparent and
impartial conict resolution (38, 4246). However, all team members, regardless of identity,
should understand their own cultural identities and biases and how they impact the team.
Towards equitable research practices, scientists from HIC should actively apply for
international grant funding opportunities which foster microbiome studies with LMIC
scientists (e.g., the NIH Fogarty International Center) and while doing so, should dis-
cuss ownership of data and authorship of publications with trainees and collaborators,
support the active participation of LMIC scientists in designing microbiome studies
and avoid helicopter researchin which HIC scientists travel to conduct research in an
LMIC with little or no involvement of local scientists. This is a practice that has become
worryingly common as global collaborations increase (47). Collaborating with, rather
than extracting from, communities or regions under study helps to decolonize science
(48). This means including LMIC and PEER scientists as coauthors and not just mention-
ing them in the acknowledgments and avoiding exploitation of their knowledge and
labor, identifying research needs for these communities, or taking local specimens
with limited engagement.
Scientists from different elds, cultures, and languages must be able to clearly com-
municate with each other to discover connections between ideas and develop sustain-
able collaborations to advance the microbiome sciences. We urge support for virtual
training programs that include efforts to create resources in multiple languages like
translation of programming tutorials of The Carpentries training organization into
Spanish. Current technology translates virtual resources and provides closed caption-
ing in real time which accommodates scientists with disabilities and nonnative speak-
ers. We also urge funding agencies and professional societies to allocate resources for
translating conference materials and to host multilingual workshops, particularly to
highlight research performed by LMIC scientists (Table 1, Microbiome training and
conference-based support for LMIC and PEER scientists). Virtual conferences have
increased access for scientists who cannot easily travel due to accessibility issues, fam-
ily commitments (49), visa requirements, and funding limitations that disproportion-
ately limit LMIC scientists participation in training, symposia, and conferences. One
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notable success has been the National Summer Undergraduate Research Program
(NSURP), a paid virtual research program that has successfully recruited microbiologists to
mentor PEER students from the United States, providing a completely online microbial
training experience and professional development opportunities (10). Since this program
currently reaches a limited number of mentees, we call for funding to expand such initia-
tives and their scope to serve trainees across geographical boundaries; increased funding
would increase the programs reach as well as allowing for international trainees to partici-
pate. For all trainees, including PEER microbiome scientists, science outreach at community
venues like schools, science centers, and museums, helps build communication skills.
Science outreach also positively impacts the communities by enhancing interest and
engagement in science and offering role models representative of studentssocial identi-
ties (50, 51), which can lead to higher recruitment of PEER scientists in STEM (science, tech-
nology, education, and mathematics) (52). We also recommend that academic programs
incentivize students with credits, certication, or awards to participate in outreach events
and science communication classes as part of their training (for examples, see Table S1 in
the supplemental material).
Microbiome data sets are large, and their analysis requires expertise in molecular
biology, microbiology, and computational biology. The extraction of nucleic acids from
samples can be done with standard molecular biology equipment, but the generation
and interpretation of these data typically require access to expensive reagents,
sequencing services, and computer clusters which is often a barrier for scientists from
LMICs. We present resources that could reduce nancial and technological barriers to
sequencing and provide free resources to high-performance computing for micro-
biome research in Table S1. These resources are primarily published modications to
standard protocols for sample preservation, DNA extraction, library preparation, and
multiplexing that reduce costs at each step in the process. Sequencing itself remains a
nancial barrier, but a few programs like the U.S. Department of Energy Joint Genome
Institutes Community Science Program provides access to sequencing and advanced
microbiome methods to scientists anywhere in the world through a grant-based, user
facility model. Free, cluster-based metagenomics computing resources are available
through Kbase, Xcede, Cyverse, MGnify, and MG-Rast (5356). In the longer term, work
should be publicly funded to develop and nonexclusively license a suite of low-cost,
validated, open-source protocols for preservation, extraction, and library preparation.
This could radically lower costs of sample preparation and thereby increase access and
equity, create new products, and open new lines of microbiome research, especially if
supported by public sector investment and technology transfer.
Microbiome data sets are large and multivariate, and analyzing these data effec-
tively requires specialized training. Data analysis training should be made accessible to
LMICs so that in silico experiments are supported alongside training of bioinformati-
cians who are comfortable using and developing projects with sequence data. We also
recommend the creation of online code clubs(57) or cross-institutional working
groups who learn to code and analyze data together. Such clubs enable peer learning,
foster opportunities for research collaborations, and provide resource and skill-sharing
between institutions with unequal economic access.
In addition to lack of access to technology, the high cost of publication in science
can be a barrier to LMIC scientists in particular (58). Some microbiome research jour-
nals offer free publication, or fee waivers or cost reductions for scientists from LMICs
(for a list of journals, see Table S2). Publishing in high-impact open-access journals con-
stitutes approximately 6 monthssalary of African scientists, and government and uni-
versities do not cover these fees (59). While fee waivers exist, the processes are veiled
and need transparency, and other journals, including society journals, must consider
providing free publishing mechanisms. Sharing research as preprints is now standard
practice in elds like physics, and microbiome research would benet from a similar
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adoption. Preprints offer the opportunity to make research rapid and more transpar-
ent, though they may require careful evaluation prior to being peer reviewed.
Open science will allow PEER and LMIC trainees to learn key data analysis skills, con-
tribute new research, and further their careers through the meta-analysis of previously
published microbiome data in the absence of funding to produce new data. However,
this requires both freely available data sets and high-quality metadata. Some federal
agencies are addressing issues associated with data accessibility by recommending
data sharing upon request (60). Transparency can also be reinforced by making sure that
accepted manuscripts provide accessible, high-quality, accessioned raw data and provide
metadata spreadsheets compatible with microbiome data management software (e.g., for
Qiita and European Bioinformatics Institute [EBI]). Funding agencies, journals, and reposito-
ries should require and provide incentives to enforce high-quality submission standards,
allow data sets to be cited, and provide better tutorials and consistent submission expecta-
tions across databases to normalize open-science practices for microbiome data (61).
Shifting the research culture in microbiome science by making research and train-
ing more inclusive will improve retention of underserved scientists and contribute to
the elds intellectual growth. Such endeavors are opportunities to broaden our per-
spectives of how the environment, social identity, biopsychosocial factors, and cultural
practices affect microbiome science around the world but are also imperative to
restore equity and social justice in the eld. We urge collaborators, mentors, funders,
and decision-makers in resource-rich countries to take concrete actions to improve the
inclusiveness of microbiome science (Fig. 1). Changing cultural norms can take time,
but implementing even small improvements can create a considerable difference for a
trainee or collaborator. As microbiome scientists, we call on other members of the
community to set an example of inclusivity and accessibility for the broader scientic
Supplemental material is available online only.
TEXT S1, DOCX le, 0.02 MB.
TABLE S1, DOCX le, 0.01 MB.
TABLE S2, DOCX le, 0.02 MB.
TABLE S3, DOCX le, 0.02 MB.
We thank Ana Maldonado-Contreras, Monika Oli, and Maria Gloria Domínguez-Bello
for discussion and ideas for this article. We thank Ben Wolfe, Emily Delorean, and Ashley
Schoon for feedback for reviewing drafts of this paper.
A.J.K. is supported in part by KL2TR002241 and UL1TR002240. A.J.F. is supported in
part by an appointment to the Agricultural Research Service (ARS) Research Participation
Program administered by the Oak Ridge Institute for Science and Education (ORISE)
through an interagency agreement between the U.S. Department of Energy (DOE) and
the U.S. Department of Agriculture (USDA). ORISE is managed by ORAU under DOE
contract number DE-SC0014664.
The ndings and conclusions in this publication are those of the authors and should
not be construed to represent any ofcial determination or policy of the USDA, U.S.
Government, or any of the entities which contributed funding.
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... Planning dietary interventions in free-living humans poses additional challenges related to timing of intake, adherence, and sampling (85). non-industrialized, and rural populations in microbiome research so that the societal benefits of precision nutrition and healthcare are more equitably distributed (22,66,89). ...
... Furthermore, it is unclear whether or not precision nutrition models trained on relatively affluent developed-world cohorts are broadly applicable to the rest of the world, necessitating a sharper focus on running observational and interventional trials in indigenous, non-industrialized, and rural populations (22,66,89). ...
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Humans often show variable responses to dietary, prebiotic, and probiotic interventions. Emerging evidence indicates that the gut microbiota is a key determinant for this population heterogeneity. Here, we provide an overview of some of the major computational and experimental tools being applied to critical questions of microbiota-mediated personalized nutrition and health. First, we discuss the latest advances in in silico modeling of the microbiota-nutrition-health axis, including the application of statistical, mechanistic, and hybrid artificial intelligence models. Second, we address high-throughput in vitro techniques for assessing inter-individual heterogeneity, from ex vivo batch culturing of stool and continuous culturing in anaerobic bioreactors, to more sophisticated organ-on-a-chip models that integrate both host and microbial compartments. Third, we explore in vivo approaches for better understanding personalized, microbiota-mediated responses to diet, prebiotics, and probiotics, from non-human animal models and human observational studies, to human feeding trials and crossover interventions. We highlight examples of existing, consumer-facing precision nutrition platforms that are currently leveraging the gut microbiota. Furthermore, we discuss how the integration of a broader set of the tools and techniques described in this piece can generate the data necessary to support a greater diversity of precision nutrition strategies. Finally, we present a vision of a precision nutrition and healthcare future, which leverages the gut microbiota to design effective, individual-specific interventions.
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Generations of colonialism, industrialization, intensive agriculture, and anthropogenic climate change have radically altered global ecosystems and by extension, their environmental microbiomes. The environmental consequences of global change disproportionately burden racialized communities, those with lower socioeconomic status, and other systematically underserved populations. Environmental justice seeks to balance the relationships between environmental burden, beneficial ecosystem functions, and local communities. Given their direct links to human and ecosystem health, microbes are embedded within social and environmental justice. Considering scientific and technological advances is becoming an important step in developing actionable solutions to global equity challenges. Here we identify areas where inclusion of microbial knowledge and research can support planetary health goals. We offer guidelines for strengthening a reciprocal integration of environmental justice into environmental microbiology research. Microbes form intimate relationships with the environment and society, thus microbiologists have numerous and unique opportunities to incorporate equity into their research, teaching, and community engagement.
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Social and political policy, human activities, and environmental change affect the ways in which microbial communities assemble and interact with people. These factors determine how different social groups are exposed to beneficial and/ or harmful microorganisms, meaning microbial exposure has an important socio-ecological justice context. Therefore, greater consideration of microbial exposure and social equity in research, planning, and policy is imperative. Here, we identify 20 research questions considered fundamentally important to promoting equitable exposure to beneficial microorganisms, along with safeguarding resilient societies and ecosystems. The 20 research questions we identified span seven broad themes, including the following: (i) sociocultural interactions; (ii) Indigenous community
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The peer-reviewed scientific literature is the bedrock of science. However, scientific publishing is undergoing dramatic changes, which include the expansion of open access, an increased number of for-profit publication houses, and ready availability of preprint manuscripts that have not been peer reviewed. In this opinion article, we discuss the inequities and concerns that these changes have wrought.
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The racialized structure of STEM (science, technology, engineering, mathematics) higher education maintains gross inequities that are illustrative of structural racism, which both informs and is reinforced by discriminatory beliefs, policies, values, and distribution of resources. Thus, an examination into structural racism in STEM is needed to expose the marginalization of underrepresented groups in STEM and to improve understanding of the STEM policies, practices, and procedures that allow the foundation of racism to remain intact. I argue that, even at the top of the education hierarchy, Black STEM doctorate students and PhD degree holders consistently endure the racist residue of higher education institutions and STEM employers. Thus, this manuscript also discusses how universities institutionalize diversity mentoring programs designed mostly to fix (read “assimilate”) underrepresented students of color while ignoring or minimizing the role of the STEM departments in creating racially hostile work and educational spaces. I argue that, without a critical examination of the structural racism omnipresent in the STEM, progress in racially diversifying STEM will continue at a snail’s pace.
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Scientific conferences have an important role in the exchange of ideas and knowledge within the scientific community. Conferences also provide early-career researchers with opportunities to make themselves known within their field of research. Although the COVID-19 pandemic has brought traditional in-person conferences to a halt for the foreseeable future, the growth of virtual conferences has highlighted many of the disadvantages associated with the in-person format and demonstrated the advantages of moving these events online. Here, based on data from in-person and virtual conferences in a range of subjects, we describe how virtual conferences are more inclusive, more affordable, less time-consuming and more accessible worldwide, especially for early-career researchers. Making conferences more open and inclusive will provide both immediate and long-term benefits to the scientific community.
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Many microbiologists exhibit a fascination with unculturable bacteria. This intrigue can be expressed through curiosity about nutrient needs, as well as about parameters such as optimal temperature, oxygen levels, minimum and optimal light, or other such environmental factors. Microbiologists study organisms’ genetic language, as well as their environment of origin, for clues about essential factors or organisms’ need for coculture to support growth and thriving. We can learn many lessons about equity and stewardship-based engagement from the ways that microbiologists seek to understand how to cultivate unculturable bacteria, including the importance of understanding an organism’s language and community, replicating aspects of the environment of origin, an organism’s occasional need to transform aspects of its environment to persist, and the critical needs to provide a range of culture conditions to support diverse organisms. These lessons from the bacterial world provide guidance applicable to addressing human inequity in scientific communities, and beyond.
Open access to the scholarly literature is crucial for African academics but, without urgent action, the move from paywall to pay-to-publish wall will continue to disenfranchise researchers. In an unpublished study, we looked at the 40 journals with the highest impact factors in our field (ecology), and found that the average article-processing charge was US$3,150. Three‑quarters of these journals do not offer waivers for scientists from low-income nations. The waiver process is complicated and opaque, and often seems to be based on special pleading. African governments and universities rarely, if ever, fund article-processing fees. Most African scientists cannot afford to pay these fees themselves. Average monthly salaries are, for example, $531 in Madagascar and $365 in Ethiopia. In Uganda, the cost of publishing two articles could cover a year’s tuition and field expenses for a master’s student. In Nigeria, the fees for one paper could cover the costs of three master’s students. We applaud the efforts of funders and publishers who are promoting the accessibility of research and creating a more equitable process. To grapple with the challenges Africa faces, building research capacity depends on scientists being able to publish in — as well as read — journals.
In response to COVID-19, universities and other education providers pivoted rapidly from in-class learning to digital course instruction. Student tuition was deemed essential, thus swift change ensued. Similarly, if equity, diversity and inclusion are truly deemed essential at those same institutions, change could occur now — not later.