Titles and abstracts of scientific reports ignore variation among species.

An analysis of more than 1000 research articles in biology reveals that the name of the species being studied is not mentioned in the title or abstract of many articles. Consequently, such data are not easily accessible in the PubMed database. These omissions can mislead readers about the true nature of developmental processes and delay the acceptance of valid species differences. To improve the accuracy of the scientific record, I suggest that journals should require that authors include the name of the species being studied in the title or abstract of submitted papers.

One undeniable truth that should be apparent to all scientists is that evolution is a tinkerer (Jacob, 1977, 2001). Such tinkering is responsible for the huge variations in the ways that organisms carry out their essential functions. We have become aware of species differences in DNA content (Atkin et al., 1965), DNA methylation (Bird, 2002), sex determination (Sander van Doorn, 2014), staging of embryonic stem cells (Ginis et al., 2004; Silva et al., 2008), length of gestation (Migeon, 2014), dosage compensation (Migeon, 2011), telomere length (Tackney et al., 2014), the repair of chromosome breakage (Doseth et al., 2011), ease of transformation (Rangarajan and Weinberg, 2003) and expression of inborn errors (Elsea and Lucas, 2002) among many other variations. This is true not only for different evolutionary kingdoms, classes, phyla, orders, but also for genera, and even among species. Such variations are attributable not only to random mutations, but also to the striking disparity in the staging of embryonic development between species. Species differences should not be ignored because they tell us so much about the determinants of these developmental events. Therefore, a mouse is a mouse and not a human surrogate.

For many years I have been surprised to see that the titles of many papers in my own field, X inactivation, do not indicate the mammalian species used for their research, implying that their evidence applies to all mammals. Many readers cannot help but assume that it does, even when other published evidence indicates that such an assumption is erroneous. Not even Xist, the mammalian non-coding RNA that recruits chromatin modifiers to inactivate X chromosomes, is present in all mammals (Duret et al., 2006). During mammalian evolution, invasions of repetitive DNA sequences have destroyed some genes in the X inactivation center, and other genetic elements have arrived on the scene (Migeon et al., 2001).

I wondered if species variation were being ignored in studies of other biological phenomena—that is, if this were a common feature of the science being reported at this time. Therefore, I examined the tables of contents of various journals to find articles and reports concerning biological subjects, scoring each with respect to inclusion of the species studied in the title and in the abstract of the paper. If the species was not mentioned in the title I looked for it in the abstract. If not mentioned there, I then looked at the experimental methods or supplementary material to find the true subjects of the study. Note, my analysis did not require a specific species, only the kind of organism studied; the words Bacteria or Yeast were as acceptable as E. coli or S. cerevisiae. When I repeated this exercise 2 years later I also asked if the experimental models were mentioned in other summary material provided by the journal. My observations are summarized in Table 1 and in the text below.

Table 1.

Is the species name mentioned in the title, impact statement, abstract and digest of eLife papers (July–Sept 2014)?

Frequency of inclusion of species in titles and abstracts of published papers

DOI: http://dx.doi.org/10.7554/eLife.05075.002

DOI: http://dx.doi.org/10.7554/eLife.05075.003

Journal	Issues	# of articles*	Is the species included in the title?			If not included in the title, is the species included in the abstract?			Species not included in title or abstract%
			Yes	No	% No	Yes	No	% No
Nature Genetics	Jan–Apr 2012	52	19	33	65	24	9	27	17
	June–Sept 2014	60	20	40	67	32	8	20	13
Cell	Feb–May 2012	96	13	83	90	46	37	45	39
	July–Sept 2014	82	18	64	78	29	35	55	43
Science	Mar–May 2012	54	22	32	59	21	11	34	20
	July–Sept 2014	59	29	30	51	20	10	33	17
PNAS	Mar–May 2012	252	111	141	56	72	69	49	27
	July 2014	119	49	70	59	36	34	49	29
PLOS Genetics	Apr–May 2012	107	56	51	48	46	5	10	5
	Aug–Sept 2014	82	44	38	46	31	7	18	9
Hum Mol Genetics	Apr–June 2012	67	26	41	61	35	6	15	9
eLife	Mar–June 2014	105	23	82	78	34	44	54	42
	July–Sept 2014	93	27	66	71	32	34	52	37

Only biological articles are included.

These data clearly show that at least half the time, the species being studied does not appear in the title; and it does not appear in the abstract either in a significant fraction of papers (Table 1). At times I had to look at the supplementary material to discover the organism studied. The ‘In Brief’ statements published in Cell and the ‘Impact Statements’ published in eLife were even less likely to reveal the species studied: 72% of In Brief statements and 86% of Impact Statements did not mention the species examined (data not shown). Moreover, 45% of ‘Digests’ published by eLife did not mention the species being studied (see Table 1—Source data 1). I also noted that Drosophila, Caenorhabditis elegans and Arabidopsis were most frequently mentioned in the title of reports about them, whereas rats and mice appeared infrequently.

Two of the journals surveyed (PNAS and eLife) include keywords that are accessible in PubMed and other databases (such as EMBASE): these keywords can include the names of the species under study, but this is not always the case. Although information about species can be captured by searching databases, readers should not have to. Species variation is key to the interpretation of findings, so the species used for the investigation should be a fundamental part of the resulting research paper and not something that can be discovered by searching an outside database.

I wondered why one has to go to the methods section (not included in the PubMed database) to find the subject of a study. Although in some cases, the function studied may be highly conserved and non-variant, often, species variations should be expected, even in conserved developmental processes. In some cases authors may be trying to make it difficult for those who abhor animal experimentation to know the subject of their study. This is most evident when non-human primates are used for the studies. But, my data suggest that often, the investigators, even if aware of species variation, do not consider it relevant enough to include in title or abstract. We need to be mindful that not including the subject of the study in the title or abstract implies that the results of the study are generally applicable to all species.

Ignoring species variation would be understandable and perhaps tolerable if it didn't lead to misinterpretation of experimental observations. I know best the upshot in my own field: It took more than 30 years for the scientific community to accept valid evidence that humans are not like mice with respect to the details of X inactivation. Because of expectations that this developmental process would be similar among mammals, it has taken too many years and costly repetitive experiments for the community to accept the evidence that humans, unlike mice do not have paternal imprinting of X-linked genes in their placental tissues (Migeon and Do, 1979; Moreira de Mello et al., 2010). Papers that do not mention mice, the species being studied, in their title or abstract (Chelmicki et al., 2014; Payer and Lee, 2014) continue to report mechanisms that have no consequence for humans or other mammals as the targeted non-coding RNA being reported in rodents is not functional in other mammalian species.

Ignoring species variation leads to over-interpretation of data, which may actually stifle novel discoveries in other organisms. Ignoring species variations is a common oversight that needs to be remedied. To improve the accuracy of the scientific record, I suggest that all journals should require that authors include the name(s) of the species being studied in the title or abstract of submitted papers.

eLife posts the editorial decision letter and author response on a selection of the published articles (subject to the approval of the authors). An edited version of the letter sent to the authors after peer review is shown, indicating the substantive concerns or comments; minor concerns are not usually shown. Reviewers have the opportunity to discuss the decision before the letter is sent (see review process). Similarly, the author response typically shows only responses to the major concerns raised by the reviewers.

Thank you for sending your work entitled “Titles and Abstracts of Scientific Reports Ignore Species Variation” for consideration at eLife. Your article has been favorably evaluated by the Features Editor (Peter Rodgers) and two reviewers, one of whom, Ferric Fang, has agreed to reveal his identity.

The Features Editor and the reviewers discussed their comments before we reached this decision, and the Features Editor has assembled the following comments to help you prepare a revised submission.

The author of this Comment notes that, in the field of X inactivation, the importance of species variation has often been ignored by researchers. To test whether this might be true of other fields, she then asks whether the species examined in experimental studies is specifically mentioned in the titles and abstracts of recent publications in several prominent journals. She reports that species are not mentioned in the titles of the majority (63%) of articles and are often (25%) not mentioned in either the title or abstract. She suggests that this has had 'detrimental consequences for the scientific community'.

We wholeheartedly agree with the author that distinctions between species can be important. For instance, the question of whether mouse models of inflammation are relevant to humans has been hotly debated (Seok et al., PNAS, 2013; Takao and Miyakawa, PNAS, 2014). However we are not convinced that the failure to mention a species name in the title and abstract necessarily indicates that the importance of species differences has been neglected (see points 1 and 2 below). And while the article is brief, it could be shortened even further to focus on its core message (see points 3-5 below).

1) Please mention that two of the journals surveyed (PNAS and eLife) include keywords, which are easily accessed in PubMed and often include the names of the species under study. Please also mention that information about species can be captured by search strategies, as databases such as EMBASE index articles by species, and even include sub-classification by experimental animal model, cell or tissue (for articles published since 1978).

2) The article should be reworded to make clear that the fact that species are not mentioned in titles does not mean that species differences are being neglected by authors. (To make the case that species differences have been neglected to the detriment of science, the author would have to go beyond the mere failure to mention species and provide specific examples in which this is the case. Otherwise one cannot exclude the possibility that authors sometimes fail to mention individual species when they wish to emphasize a highly conserved phenomenon that is generalizable across many species. For instance, rRNA, tRNA and nucleotide binding domains of ABC transport proteins are highly conserved in all kingdoms of life, and it might not necessarily be essential or relevant to designate an individual species in the abstract of an article that is attempting to make a general point. For example, the article 'Molecular Architecture of a Eukaryotic Translational Initiation Complex' (Fernandez et al. Science, 2013) might be criticised by the author as neglecting to mention that the study was performed in S. cerevesiae, but in fact the authors note throughout the paper that this mechanism is conserved from bacteria to humans.)

3) Passages that make various assumptions about why species are not mentioned in titles/abstracts should be removed. These include the sentence “This practice is based [. . .] is erroneous”, and the passage “I suppose that in some cases […] in prestigious journals.”

4) The column containing impact factors should be removed from Table 1; impact factors are not mentioned in the article and don't seem relevant to the points being made. And in any case, our official eLife policy is to eschew the use of impact factor in any discussion of scholarly assessment.

5) Table 2 should be deleted, and the relevant section of the text should be modified accordingly. Much of the data in Table 2 already appears in Table 1; regarding the new data, it is not clear that one would expect, say, the graphical abstracts published by Cell or the Digests published by eLife to contain species information. (Note from Peter: the Digests in eLife are aimed at the general public, so they will often refer to, say, bacteria or yeast, rather than to specific species.)

1) Please mention that two of the journals surveyed (PNAS and eLife) include keywords, which are easily accessed in PubMed and often include the names of the species under study. Please also mention that information about species can be captured by search strategies, as databases such as EMBASE index articles by species, and even include sub-classification by experimental animal model, cell or tissue (for articles published since 1978).

I have included the following in my comment: “Two of the journals surveyed (PNAS and eLife) include keywords that are accessible in PubMed and may, but do not always include the names of the species under study. Although information about species can be captured by search strategies, such as EMBASE, readers should not have to, and do not often consult these databases for the purpose of determining the species under study. Because species variation is key to the interpretation of findings, the species used for the investigation should be a fundamental part of reportage and not something that can be discovered by searching an outside database.”

2) The article should be reworded to make clear that the fact that species are not mentioned in titles does not mean that species differences are being neglected by authors.

My data suggest that often investigators, even if aware of species variation, do not consider it relevant enough to include species name in Title or Abstract.

(To make the case that species differences have been neglected to the detriment of science, the author would have to go beyond the mere failure to mention species and provide specific examples in which this is the case […]

I did mention the 30-year delay in convincing the scientific community of the validity of species differences in placental imprinting of X inactivation. And that key players in one species may not be present in others, making the observations less important than advertised, as they do not explain what is going on in most mammals.

[…] Otherwise one cannot exclude the possibility that authors sometimes fail to mention individual species when they wish to emphasize a highly conserved phenomenon that is generalizable across many species. For instance, rRNA, tRNA and nucleotide binding domains of ABC transport proteins are highly conserved in all kingdoms of life, and it might not necessarily be essential or relevant to designate an individual species in the abstract of an article that is attempting to make a general point. For example, the article 'Molecular Architecture of a Eukaryotic Translational Initiation Complex' (Fernandez et al. Science, 2013) might be criticised by the author as neglecting to mention that the study was performed in S. cerevesiae, but in fact the authors note throughout the paper that this mechanism is conserved from bacteria to humans.)

I agree that such variation is a moot point when there is no variation. But some assumptions of conservation need to be documented.

3) Passages that make various assumptions about why species are not mentioned in titles/abstracts should be removed. These include the sentence “This practice is based […] is erroneous”, and the passage “I suppose that in some cases […] in prestigious journals.”

I have revised the offending passages.

4) The column containing impact factors should be removed from ; impact factors are not mentioned in the article and don't seem relevant to the points being made. And in any case, our official eLife policy is to eschew the use of impact factor in any discussion of scholarly assessment.

I have removed the impact factors from Table 1.

5) Table 2 should be deleted, and the relevant section of the text should be modified accordingly. Much of the data in Table 2 already appears in ; regarding the new data, it is not clear that one would expect, say, the graphical abstracts published by Cell or the Digests published by eLife to contain species information.

I did not know what to expect and so I asked the question. As you see these extra summaries do not often provide such information: 72% of In Brief and 88 % of Graphical Abstracts published by Cell and 86 % of Impact Statements and 45% of Digests published by eLife did not mention species. Table 2 has been removed.

(Note from Peter: the Digests in eLife are aimed at the general public, so they will often refer to, say, bacteria or yeast, rather than to specific species).

My analysis did not require authors to state a specific species, only the kind of organism they were studying. Bacteria or Yeast were as acceptable as E. coli and S. cerevisiae. I added this statement in my comment.