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

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 delta(18)O and delta(13)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 similar to 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.