08 November 2006
Re:
Re-submission of manuscript ME 06-012
Subject Editor:
Professor Angus Davison
Previous Decision: Reject, Encourage
Dear Professor Harry Smith FRS, Managing Editor, Molecular Ecology,
This document provides a detailed description of the improvements we have made to the manuscript:
“The role of tropical dry forest as a potential long-term barrier to dispersal:
A comparative phylogeographic analysis of dry forest tolerant and intolerant frogs.”
By: Andrew J. Crawford, Eldredge Bermingham, and Carolina Polanía.
Below we first address the general criticisms mentioned by our two thoughtful Referees, then proceed line
by line addressing each of the more specific comments and criticisms provided by the Referees.
The general criticism of our paper may be summarised by the following quote from the Decision letter by
Professor Angus Davison, Subject Editor:
Both referees agree that this is an interesting paper containing some high quality science.
However, both also agree that it lacks clarity in parts and ideas are hard to follow. In particular
referee 1 has concerns that the dataset is quite small, too small in fact for a full length article in
Molecular Ecology.
In particular, it was pointed out that for one of our focal species, Craugastor crassidigitus, the Costa Rican
(CR) Caribbean region was represented by a single sample. As the following table shows, we now have 12
samples representing the Caribbean CR clade, and overall we have doubled the number of samples
included in the manuscript:
Previous version
Total samples in data set:
43
Total C. crassidigitus samples:
10
C. crassidigitus from Caribbean CR:
1
Total C. fitzingeri samples:
21
Total C. talamancae samples:
2
Number of ingroup species:
7
New Manuscript
89
29
13
31
10
12
We hope that the reviewers, whether old or new to this manuscript, will find this increased sampling
adequate.
We have also updated the References since our original submission on 25 December 2005. We have added
seven citations from 2006 in this new manuscript.
Addressing comments of REFEREE 1.
Referee 1 was overall rather complimentary to our manuscript,
The data was thoroughly analyzed and, although the dataset was quite small, it broadly
supported the author’s conclusion. Indeed, I see no major flaw with the data nor the
conclusions. Much of it is quite interesting and could be of broad general interest to the readers
of Molecular Ecology.
but had two specific criticisms. The first criticism was that the paper was not compelling enough to warrant
a full-length paper. We hope with the 2-fold increase in sampling that this referee might find our revised
manuscript more compelling. The second criticism was:
The Discussion, in particular, needs to be focused considerably. As it stands, it quite fractured
and diffuse and appears to be a series of statements crudely assembled in a humpty-dumpty-like
style.
The second Referee had a similar criticism along with some specific comments for improving the
manuscript, so we would like to address this issue below.
Addressing comments of REFEREE 2.
Referee 2 gave our manuscript the favourable review of “Accept after minor revision.” The major
comment from Referee 2 was that “The organization and flow of the discussion could be improved” and
this person generously gave various suggestions on how this could be accomplished. Below we address the
minor comments first, then tackle the larger comments.
Line 82 – missing a be?
This was true. Now fixed.
Line 87 – tropical dry forest is one barrier – are the mountains a second? Good point. We add the
following italicized text to the sentence in question: “... to investigate the relative roles of mountains and
tropical dry forest habitat in shaping the distribution of wet-forest frogs on the Pacific and Caribbean
versants of lower Central America (Fig. 1).”
Line 98 – 103 – you mention frogs but give no examples – seems odd. Good point, especially since at
this point in the text we have not introduced the frogs under investigation here. We added the sentence:
“Frog species that show this disjunct pattern include Bufo haematiticus (Bufonidae), Dendropsophus
ebraccatus and Smilisca phaeota (Hylidae), as well as Craugastor crassidigitus (Brachycephalidae)
(Savage 2002).”
Line 103 – this history/geography of the region should be in the same paragraph (i.e., you have more
starting on line 109 and 117).... Good point. We adjusted the paragraph breaks accordingly.
... I also wonder if it would be helpful to set the stage by describing the region and then the patterns
of genetic structure you see in different taxonomic groups for that region. We tried this approach, but
we feel that it is important to first motivate the description of the region. Therefore, we describe the curious
geographic distribution and list some members of the vertebrate fauna that share this pattern. This shared
pattern then motivates our description of the environmental features of the region. (Note, we are not giving
examples of previous studies of “genetic structure,” rather we can only provide examples of other species
that share the “disjunct” pattern in their geographic distribution between Pacific and Caribbean coasts.)
In summary, we organise the Introduction as follows, by paragraph: 1) ecology vs. history in the evolution
of species’ ranges. 2) A curious pattern of geographic distribution shared among species: continuous
Caribbean + isolated Pacific populations. 3) The geographic features that account for this distribution. 4)
Introducing the study organisms and their ecologies. 5) Some hypotheses. 6) Our predictions. We hope
this structure is readable and agreeable to the referees.
Line 143 – can you cite this? Note, in our new draft we moved this sentence from the Introduction to the
Discussion, so that all discussion of habitat differences among species is found in one place. But to answer
this question from Referee 2: Unfortunately, there are not enough quantitative studies of frog abundance in
this region, and the best data we have are actually misleading. Lieberman (1986) surveyed plots in the leaflitter at La Selva, Costa Rica, where all three species co-occur: Craugastor crassidigitus, C. fitzingeri, C.
talamancae). Among 1,427 amphibians found, the counts for these three species were 2, 2, 25, respectively.
However, C. fitzingeri is not typically found on the forest floor where the “plots” are inventoried. Thus,
these data belie the general consensus among herpetologists that C. fitzingeri is actually quite abundant, as
evidence by the fact that they are easy to locate in bushes or by following their advertisement calls.
The material/methods and results seem fine. Thank you!
Discussion – General comments:
The organization and flow of the discussion could be improved. All geographic breaks, filter barriers
etc. need to be on a map – esp. the Bocas del Toro barrier – include in figure 1 or 2? Good suggestion.
Fig. 2 now includes a large orange arrow indicated the location of the “Bocas del Toro filter barrier.”
I would greatly reduce the first paragraph as it is redundant with the rest of the discussion. I would
consider a different word on line 486 for “phylogenetic control” – does this mean conservatism or is
there a way to say this that is less ambiguous? Good points. We simply deleted this first paragraph.
Also, we removed the ambiguous term “phylogenetic control” from the manuscript.
For example, Page 12, line 495 to 515: The argument flows from the level of genetic diversity, to a
statement of the two possible reasons for this diversity (gene flow and recent expansion), to age of
common ancestors, to discussion of pattern, back to level of genetic diversity, to a question, to a
broad statement that does not really fit in, back to a statement about age, to a statement about
ecology. We appreciate these comments form Referee 2, and we have made extensive revisions and
reductions to the opening paragraphs of the Discussion. See replies to specific comments below.
In these paragraphs I also find confusing the statement that C. fitz is as old as C. crass when in the
previous paragraph we are told that C. fitz has a common ancestor in the Pleistocene and C. crass in
the Miocene. We deleted the former comment: “...permits us to infer that C. fitzingeri is at least as old as
C. crassidigitus...”.
It might be best to start with the broad statement “A myriad...”, though I do not understand how the
comment about caution fits in – perhaps better would be a careful/simultaneous evaluation of a series
of traits. I would then discuss each of the different factors – age, genetic structure and ecology and
how these factors together allow you to draw certain conclusions. Good points. We have reduced and
hopefully clarified the discussion. Instead of “A myriad”, we focus on three factors that may influence
phylogeographic structure: “environmental history, the unique evolutionary history of the species, and the
species’ autecology.” We then suggest that the first two factors are of minimal explanatory power in
accounting for the differences in phylogeographic structuring among species, because our three focal
species are both broadly sympatric and are each other’s closest relatives.
The ecology starting on line 517 is explained well – age and genetic structure and perhaps geography
should also have similar well-explained paragraphs. Thank you. We have moved this paragraph up to
an earlier position in the Discussion. In the remainder of the Discussion, we have endeavoured to reduce
the redundant information by combining similar topics. See further comments and changes outlined below.
The ecology vs history section (line 534) is somewhat redundant with earlier ideas presented in the
discussion. Also, I find the statement that differences in habitat preference increase the potential for
allopatric speciation a bit confusing – this needs to be stated/explained more explicitly. I am not sure
this paragraph warrants a section heading. We have removed this section heading. We shortened this
paragraph, removed the discussion of the potential for allopatric speciation, and combined the remaining
text with the preceding section heading “comparative phylogeography.” To further reduce potential
redundancy, we focus this paragraph on species ranges while the previous paragraph was focused explicitly
on the extent of phylogeographic structure.
Much of the information on page 14 is also on page 15 – for example line 600 is about past climate
and vegetation as is line 630. I would suggest significant restructuring of this and the previous
section so that the reader has one clear message about the type of vegetation, uplift of mountains and
how timing of these events relates to the phylogenetic structure. Good points. We removed all the
information on historical environments as well as the mention of previously published studies from the
revised section now entitled “The origin of the Golfo Dulce populations.” This section now focuses
exclusively on understanding the results of our focal species. We moved the historical, environmental and
comparative information to the subsequent section entitled “Craugastor as a model for the origin of the
Golfo Dulce fauna”. In this revised section we start with the historical and environmental context to
interpret the current results, and then we bring in examples from the literature. We hope this revised
structure will be clearer to the reader as well as more concise.
I am not convinced of the statement on line 649 – what if the regions were been connected during a
short period and the generalist species also had greater dispersal abilities so it could “take
advantage” of this connectivity? Referee 2 is quite correct to point out this possibility. Therefore, we
added three sentences: “Our estimated age for the drying of the Pacific slope of western Panama is notably
older than the interval 1-2 Ma suggested by McDiarmid and Savage (2005). While there may have been
brief intervals during the Pleistocene in which wet forest might have become established and yet C.
crassidigitus simply failed to move through the region, the historical data and current environmental
reconstructions do not support this hypothesis (Piperno and Pearsall 1998). Further comparative
phylogeographic studies should help resolve this issue.”
The final sentence (line 659) requires a little more context. Very good point. We now preface our
concluding sentence with this paragraph: “The phylogeographic histories of C. fitzingeri and C.
crassidigitus may reflect a general relationship of the Golfo Dulce fauna to neighbouring regions. Further
studies of this region will determine if the local community is comprised of an assemblage of young
lineages within generalist species, like C. fitzingeri, mixed with deeply structured phylogeographic
representatives of wet forest specialists, like C. crassidigitus. The Golfo Dulce region hosts 156 species of
reptile and amphibian (Savage 2002). At least twelve of these species are endemic, while most of the
remaining species are shared with Caribbean Costa Rica or central Panama (McDiarmid and Savage
2005). Our success in this endeavour, however, will depend on an accurate understanding of species
diversity and its origins, something that is still lacking in Neotropical batrachology (the study of
amphibians) (e.g., Ron et al. 2006). In the current study we included 3 undescribed highland taxa, one of
which may well be extinct already (see Lips et al. 2006). Some our known highland species may be gone as
well. For example, C. cuaquero is known only from the type locality, the site of drastic amphibian decline
(Pounds and Crump 1994; Pounds et al. 1997) while C. andi and C. escoces are both listed as “Critically
Endangered” and “possibly Extinct” by the Global Amphibian Assessment (IUCN et al. 2004). Finally, ...”
and here we add the final sentence but slightly modified:
“... the magnitude of intraspecific genetic distance revealed here for “known” lowland species, C.
crassidigitus and C. talamancae, underscores how much tropical amphibian diversity and evolutionary
history yet remains obscured by current taxonomy (e.g, Stuart et al. 2006).”
Thank you very much for your time and your consideration of this manuscript.
Andrew J. Crawford
Communicating author, ME 06-012
Email: andrew@dna.ac