Evolutionary mechanisms for camouflage in Cladomorphus phyllinus (Phasmatodea): A reflection on the role of evidence for hypotheses proposition

Abstract

We address and discuss some of the many flaws exhibited by Costa et al. (2019) which tried to explain the twig-like camouflage of Cladomorphus phyllinus. Given the lack of both empirical and theoretical underpinnings in Costa et al. (2019), we call into question the validity of their conclusions, in particular, that horizontal gene transfer is a causal mechanism for the camouflage in C. phyllinus.

Key words
Hemiptera; lateral gene transfer; stink bug; walking-stick insect

INTRODUCTION

“Extraordinary claims require extraordinary evidence.” ― Carl Sagan

In a recent paper, Costa et al. (2019) [from now on CEA] offer a report on the predation of a species of predatory stink bug [Supputius cincticeps (Stål, 1860) (Hemiptera, Pentatomidae, Asopinae)] over a walking-stick insect [Cladomorphus phyllinus Gray, 1835 (Phasmatodea, Phasmatidae, Cladomorphinae)]. The paper presents natural history observations on this interaction but further proposes an astonishing claim: that the twig aspect of this species of Phasmatodea could have arisen through horizontal gene transfer (HGT) of a morph plant gene via the stink bug. Given that very little is known about the mechanisms of morphogenesis in animals, and in insects in particular, any hypothesis of evolutionary camouflage mechanism in walking-stick insects invoking a morphogene should be adequately substantiated. Here, we present some arguments that doubt the validity of CEA statements and strongly reject the notion of these statements being scientific hypotheses.

DISCUSSION

In their paper, CEA claimed that their observations are the first report of predation between Asopinae over Phasmatodea; nonetheless records of predator-prey interaction between Asopinae and Phasmatodea go back more than a century (e.g., Kirkland 1898), and interactions between Asopinae species and their prey are opportunistic (de Clercq 2000). The interaction documented by CEA thus seems to be casual and uncommon given that it was carried out under laboratory conditions and based on a single observation of a S. cincticeps nymph.

The core of CEA paper presented an alternative idea on how camouflage could have evolved in Phasmatodea, different from the evolution of masquerade camouflage (Skelhorn et al. 2010, Dias Lima & Kaminski 2019). The authors weave assumptions related to zoophytophagy, HGT, and camouflage to speculate a causality link between the predation of S. cinctipes over C. phyllinus, and the particular phenotype of this species of Phasmatodea. With such a great claim, the reader could expect a careful exposition of theories and correct use of methods and techniques designed to explore in-depth the morphological, behavioral, and molecular data involved in this predator-prey system (e.g., Lin et al. 2016, Gao et al. 2018). Unfortunately, this was not the case. Instead, CEA relied on non-supported ideas to substantiate their unusual claim. CEA invoked HGT from a plant species to a Phasmatodea via a Pentatomidae predator with nonexclusive phytophagous habit. This argumentation gravely suffers from various issues. The first is that they argue that S. cinctipes need to feed on plants to complete its life-cycle. Nonetheless, the results of experimental research using only animal prey (e.g., Tenebrio molitor L., Musca domestica L.), comparing longevity, fertility, and other biological parameters (e.g., Beserra et al. 1995, Zanuncio et al. 1997, 2005, Oliveira et al. 2003) do not support this claim. Supputius cincticeps is indeed a generalist predator that may have an advantage in longevity when supplementing their diet with plant tissue (Zanuncio et al. 2004), although plant feeding is not necessary for its development. Furthermore, S. cinctipes, as well as all other asopines, are predatory species that cause the death of their prey during its feeding (Martínez et al. 2016, Walker et al. 2016), not fulfilling the goal of HGT process, which is the transfer of genetic material to another non-related organism and inserting these elements permanently. Therefore, the probability of S. cinctipes being a vector responsible for any HGT is very low.

HGT is the acquisition of genes from organisms other than a direct ancestor (Crisp et al. 2015). These transfers are common within Bacteria, Archaea, and between them (e.g., Ochman et al. 2000, Gophna et al. 2004). HGT involving Eukarya is more uncommon than compared to prokaryotes (Syvanen 2012). Although it is a highly complex process, given that the transmitted genes must be introduced in germline cells (Blaxter 2007), successful HGT cases have been documented in Animalia (e.g., Moran & Jarvik 2010, Walsh et al. 2013), Plantae (e.g., Baidouri et al. 2014), and Fungi (e.g., Novikova et al. 2010). However, even genes successfully transmitted and integrated into an organism are not necessarily transcribed in the recipient cell (Nikoh et al. 2008). A few instances of HGT involving retroelements of plants and arthropods are known, involving genomic elements from arthropods to spermatophytes (Lin et al. 2016, Gao et al. 2018), as well as from plants or fungi into arthropods (e.g., Moran & Jarvik 2010, Altincicek et al. 2012, Zakharov 2016). In all instances of HGT involving arthropods, there is no consensus as to how the process was achieved (e.g., Wybouw et al. 2012), but always involved genes only with particular metabolic functions (Grbić et al. 2011, Wybouw et al. 2012, Nováková & Moran 2012). Thus, it is assumed that HGT in arthropods will correspond to very specific gene functions.

The most critical and flawed argument of CEA paper is that the camouflage exhibited by C. phyllinus is the result of HGT “of plant-derived genetic material leading to development of a form resembling a tree stem”. This assumption is highly problematic in several respects. First, very little is known about the control of plant morphology. A fundamental question in plant biology is how different plant phenotypes arise based on particular genetic information, and how the environment interacts with this information to produce distinct phenotypes. Although this question is just starting to be answered (e.g., Schlichting & Pigliucci 1993, Yang et al. 2014, Casacuberta et al. 2016, Gaudinier & Brady 2016, Honkanen et al. 2016), it is clear, as recent research suggests, that plant phenotypes are the result of polygenic control (Ogura & Busch 2016, Bucksch et al. 2017), and thus must be assumed that several loci are responsible in producing particular phenotypes on specific parts of plants. CEA did not provide a plausible explanation as to how all these genetic elements were transferred and inserted into the insect. This is also highly problematic because they failed to provide a theoretical underpinning that might help explain how the whole suite of genes involved in plant morphogenesis might adequately function in another organism with radically different genetic control mechanisms. Thus, the failure is twofold, lacking both empirical evidence and theoretical support that might allow other researchers to test these ideas.

Finally, CEA implicitly expand the HGT process to other Phasmatodea, wrongly assuming that all species in the order are twig-like, which is not the case. Phasmatodea exhibit various body types, resembling various plant forms such as twigs, leaves, or moss (Bradler & Buckley 2020), and thus are probably the result of various evolutionary selective pressures, as evidenced by the various phylogenetic patterns recovered (Whiting et al. 2003, Bradler et al. 2014, Robertson et al. 2018). If HGT is responsible for the twig-like appearance of C. phyllinus, then it should have been explained how other species of Phasmatodea also present similar plant-looking body types, another idea that was never properly discussed in their paper.

CONCLUSIONS

A single observation of S. cinctipes feeding to C. phyllinus, lacking additional empirical and theoretical support, prevents to postulate HGT as the driving mechanism explaining the camouflage in this phasmatodean species. In a broad sense, scientific evidence is something that gives a scientist a good reason to consider a hypothesis true (Achinstein 2008), being this evidence filtered through a personal judgment and then interpreted as strong, weak, incomplete, redundant, inconclusive, plausible, and so on (Schum 2001). Scientific evidence gains its value not from using empirical data alone, but from how the evidence was produced, and to which theories the conclusions based on this evidence are compared to (Bogen 2017). The zenith of evolutionary biology is the building of narratives based on evidence. However, the mere concatenation of evidence in a coherent sequence attributing causality between them is not subject to confirmation or disconfirmation (Abbott 1992, Mink 1987). Regrettably, CEA paper lacks both empirical data and theoretical postulates to properly advance a scientific theory with regard to Phasmatodea camouflage. Finally, all this argumentation calls for a stronger peer-review process of our ideas submitted to scientific journals, in order to produce better science.

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Publication Dates

• Publication in this collection
  13 July 2020
• Date of issue
  2020

History

• Received
  14 Feb 2020
• Accepted
  20 Mar 2020