Cryptic speciation in the living planktonic foraminiferGlobigerinella siphonifera(d'Orbigny)

Abstract

Abstract.-Two living forms of Globigerinella siphonifera (d'Orbigny), presently identified as Type I and Type II, can easily be distinguished and collected by SCUBA divers because of differences in appearance, arrangement of the rhizopodial network, and the presence or absence of commensals. Additional biological differences are apparent from laboratory culture experiments; Type I individuals survive significantly longer than Type II under conditions of darkness and starvation and have significantly slower chamber formation rates. Stable isotopic analyses of Types I and II also reveal notable differences, with Type I consistently yielding more negative S'^O and 8"C values. Results of Mg / Ca ratio analyses indicate that Type II specimens precipitated their shells in slightly cooler (deeper) surface waters than Type I specimens. These observations and results from DNA sequencing unequivocally demonstrate that G. siphonifera Types I and II should be regarded as biological sister species.Contrarily, biometric analysis of the empty shells reveals few significant differences between G. siphonifera Types I and II. Of all the features measured from X-ray and SEM images of serially dissected specimens, only shell porosity yields readily discernible differences, with Type I adult chambers averaging 10-20% porosity and Type II adult chambers averaging 4-7% porosity. Statistically significant differences between Type I and II populations are revealed in maximum test diameter (Type I is typically larger) and coiling (Type I is typically more evolute), but these differences do not justify species level distinction of Types I and II using traditional paleontological species concepts.On the basis of the above evidence, and since all specimens were collected at the same location at ~ 3-8 m water depth, we conclude that G. siphonifera Types I and II are living examples of cryptic speciation, whereby biological speciation has occurred in the absence of discernable change in shell morphology. However, it is not clear when or where this speciation took place. Preliminary study of deep-sea cores from the Caribbean and Pacific sides of the Isthmus of Panama reveals a predominance of specimens with Type II porosity values, with rare occurrence of specimens yielding Type I porosity values. Systematic downcore measurement of shell porosity and tightness of coiling needs to be extended back to the middle Miocene, when G. siphonifera first appeared, to determine the timing of the Type I and II morphological divergence.Postulated mechanisms for reproductive isolation and speciation of Types I and II include alloparapatric, depth parapatric, and sympatric speciation. These models could be tested if further analysis of fossil G. siphonifera shells allows determination of the timing of speciation, the preferred depth distribution, and the history of geographic distribution of Types I and II.

The Diversity and Distribution of Modern Planktic Foraminiferal Small Subunit Ribosomal RNA Genotypes and their Potential as Tracers of Present and Past Ocean Circulations

“…However, it is quite possible that shell morphology may not be a true measure of planktic foraminiferal diversity. It has been demonstrated that two distinct genotypes of Globigerinella siphonifera cannot be discriminated morphologically without close analysis of test ultrastructure [Huber et al, 1997]. Clear genetic differences can be identified between genotypes in such cryptic speciation events.…”

Factors Influencing Porosity in Planktonic Foraminifera

“…In planktonic foraminifera, heritability has yet to be measured for any morphological trait, although it is likely to vary amongst traits as it does in all other organisms studied to date (Visscher et al, 2008). In this context, it is interesting to note that genetic-species of planktonic foraminifera are often found in distinct environments (i.e., different biomes or different depth habitats) (Huber et al, 1997;de Vargas et al, 2001;Darling & Wade, 2008;Morard et al, 2009;Quillévéré et al, 2011;Morard et al, 2013;Morard et al, 2016). While evidence for high heritability of wall thickness and porosity is lacking, both 325 porosity and wall thickness have been observed to vary with environmental conditions in culture and across environments gradients (this study; Colombo & Cita, 1980;Caron, 1987a-b;Bijma et al, 1990;Lea et al, 1999;Spero et al, 1997;Russell et al, 2004;Lombard et al, 2009;Kuroyanagi et al, 2013;Spero et al, 2015;Henehan et al, 2017).…”

“…This raises the interesting possibility that some of the morphological differences between different genetic species are driven primarily by differences in the environment in which they occur, rather than by heritable genetic differences. While 330 explanations of ecophenotypy have been dismissed in the past (Huber et al, 1997;Morard et al, 2009), our results suggest it should be seriously considered, at least for some traits like porosity, going forward.…”

“…Differences in porosity have been observed among genetic species within two morphospecies complexes: Orbulina universa and Globigerinella siphonifera (Huber et al, 1997;de Vargas et al, 1999;Morard et al, 2009;Morard et al, 2013;Marshall et al, 2015;Weiner et al, 2015). In fact, it is the sole characteristic by which two cryptic species of Globigerinella siphonifera can be identified in empty tests (Huber et al, 1997).…”

“…Ecophenotypy in planktonic foraminifera has largely fallen out of favor as an explanation for variation in morphology, with the observations that ecophenotypes often align with different genetic complexes (Huber et al, 1997;de Vargas et al, 1999;de Vargas et al, 2001;Morard et al, 2009;Quillévéré et al, 2011;Morard et al, 2013;Marshall et al, 2015;Weiner et al, 2015). However, it is well-established that the expression of any phenotypic trait is a product of both its genes and its environment (e.g.…”